All EyeLink Publications
All 12,000+ peer-reviewed EyeLink research publications up until 2023 (with some early 2024s) are listed below by year. You can search the publications library using keywords such as Visual Search, Smooth Pursuit, Parkinson’s, etc. You can also search for individual author names. Eye-tracking studies grouped by research area can be found on the solutions pages. If we missed any EyeLink eye-tracking papers, please email us!
2021 |
Isabell Hubert Lyall; Juhani Järvikivi Individual differences in political ideology and disgust sensitivity affect real-time spoken language comprehension Journal Article In: Frontiers in Psychology, vol. 12, pp. 699071, 2021. @article{HubertLyall2021, Individuals' moral views have been shown to affect their event-related potentials (ERP) response to spoken statements, and people's political ideology has been shown to guide their sentence completion behavior. Using pupillometry, we asked whether political ideology and disgust sensitivity affect online spoken language comprehension. 60 native speakers of English listened to spoken utterances while their pupil size was tracked. Some of those utterances contained grammatical errors, semantic anomalies, or socio-cultural violations, statements incongruent with existing gender stereotypes and perceived speaker identity, such as “I sometimes buy my bras at Hudson's Bay,” spoken by a male speaker. An individual's disgust sensitivity is associated with the Behavioral Immune System, and may be correlated with socio-political attitudes, for example regarding out-group stigmatization. We found that more disgust-sensitive individuals showed greater pupil dilation with semantic anomalies and socio-cultural violations. However, political views differently affected the processing of the two types of violations: whereas more conservative listeners showed a greater pupil response to socio-cultural violations, more progressive listeners engaged more with semantic anomalies, but this effect appeared much later in the pupil record. |
Marcus Grueschow; Nico Stenz; Hanna Thörn; Ulrike Ehlert; Jan Breckwoldt; Monika Brodmann Maeder; Aristomenis K. Exadaktylos; Roland Bingisser; Christian C. Ruff; Birgit Kleim Real-world stress resilience is associated with the responsivity of the locus coeruleus Journal Article In: Nature Communications, vol. 12, pp. 2275, 2021. @article{Grueschow2021, Individuals may show different responses to stressful events. Here, we investigate the neurobiological basis of stress resilience, by showing that neural responsitivity of the noradrenergic locus coeruleus (LC-NE) and associated pupil responses are related to the subsequent change in measures of anxiety and depression in response to prolonged real-life stress. We acquired fMRI and pupillometry data during an emotional-conflict task in medical residents before they underwent stressful emergency-room internships known to be a risk factor for anxiety and depression. The LC-NE conflict response and its functional coupling with the amygdala was associated with stress-related symptom changes in response to the internship. A similar relationship was found for pupil-dilation, a potential marker of LC-NE firing. Our results provide insights into the noradrenergic basis of conflict generation, adaptation and stress resilience. |
Josephine M. Groot; Nya M. Boayue; Gábor Csifcsák; Wouter Boekel; René Huster; Birte U. Forstmann; Matthias Mittner Probing the neural signature of mind wandering with simultaneous fMRI-EEG and pupillometry Journal Article In: NeuroImage, vol. 224, pp. 117412, 2021. @article{Groot2021, Mind wandering reflects the shift in attentional focus from task-related cognition driven by external stimuli toward self-generated and internally-oriented thought processes. Although such task-unrelated thoughts (TUTs) are pervasive and detrimental to task performance, their underlying neural mechanisms are only modestly understood. To investigate TUTs with high spatial and temporal precision, we simultaneously measured fMRI, EEG, and pupillometry in healthy adults while they performed a sustained attention task with experience sampling probes. Features of interest were extracted from each modality at the single-trial level and fed to a support vector machine that was trained on the probe responses. Compared to task-focused attention, the neural signature of TUTs was characterized by weaker activity in the default mode network but elevated activity in its anticorrelated network, stronger functional coupling between these networks, widespread increase in alpha, theta, delta, but not beta, frequency power, predominantly reduced amplitudes of late, but not early, event-related potentials, and larger baseline pupil size. Particularly, information contained in dynamic interactions between large-scale cortical networks was predictive of transient changes in attentional focus above other modalities. Together, our results provide insight into the spatiotemporal dynamics of TUTs and the neural markers that may facilitate their detection. |
Jan Grenzebach; Thomas G. G. Wegner; Wolfgang Einhäuser; Alexandra Bendixen Pupillometry in auditory multistability Journal Article In: PLoS ONE, vol. 16, no. 6, pp. e0230039, 2021. @article{Grenzebach2021, In multistability, a constant stimulus induces alternating perceptual interpretations. For many forms of visual multistability, the transition from one interpretation to another ("perceptual switch") is accompanied by a dilation of the pupil. Here we ask whether the same holds for auditory multistability, specifically auditory streaming. Two tones were played in alternation, yielding four distinct interpretations: the tones can be perceived as one integrated percept (single sound source), or as segregated with either tone or both tones in the foreground. We found that the pupil dilates significantly around the time a perceptual switch is reported ("multistable condition"). When participants instead responded to actual stimulus changes that closely mimicked the multistable perceptual experience ("replay condition"), the pupil dilated more around such responses than in multistability. This still held when data were corrected for the pupil response to the stimulus change as such. Hence, active responses to an exogeneous stimulus change trigger a stronger or temporally more confined pupil dilation than responses to an endogenous perceptual switch. In another condition, participants randomly pressed the buttons used for reporting multistability. In Study 1, this "random condition"failed to sufficiently mimic the temporal pattern of multistability. By adapting the instructions, in Study 2 we obtained a response pattern more similar to the multistable condition. In this case, the pupil dilated significantly around the random button presses. Albeit numerically smaller, this pupil response was not significantly different from the multistable condition. While there are several possible explanations-related, e.g., to the decision to respond-this underlines the difficulty to isolate a purely perceptual effect in multistability. Our data extend previous findings from visual to auditory multistability. They highlight methodological challenges in interpreting such data and suggest possible approaches to meet them, including a novel stimulus to simulate the experience of perceptual switches in auditory streaming. |
Steven M. Gillespie; Ian J. Mitchell; Anthony R. Beech; Pia Rotshtein Processing of emotional faces in sexual offenders with and without child victims: An eye-tracking study with pupillometry Journal Article In: Biological Psychology, vol. 163, pp. 108141, 2021. @article{Gillespie2021, Socio-affective dysfunction is a risk-factor for sexual offense recidivism. However, it remains unknown whether men who have sexually offended with and without child victims show differences in eye scan paths and autonomic responsivity while viewing facial expressions of emotion. We examined differences in accuracy of emotion recognition, eye movements, and pupil dilation responses between sex offenders with child victims, sex offenders without child victims, and a group of non-offenders living in the community. Sex offenders without child victims looked for longer at the eyes than sex offenders with child victims and non-offenders. Men without child victims also scored higher for psychopathy linked disinhibition, and these traits were associated with looking longer at the eyes of afraid faces. We found no evidence for group differences in accuracy, visual attention to the mouth, or pupil dilation responses. Our findings have implications for understanding the nature of socio-affective dysfunction in sexual offenders. |
Wendel M. Friedl; Andreas Keil Aversive conditioning of spatial position sharpens neural population-level tuning in visual cortex and selectively alters alpha-band activity Journal Article In: Journal of Neuroscience, vol. 41, no. 26, pp. 5723–5733, 2021. @article{Friedl2021, Processing capabilities for many low-level visual features are experientially malleable, aiding sighted organisms in adapting to dynamic environments. Explicit instructions to attend a specific visual field location influence retinotopic visuocortical activity, amplifying responses to stimuli appearing at cued spatial positions. It remains undetermined both how such prioritization affects surrounding nonprioritized locations, and if a given retinotopic spatial position can attain enhanced cortical representation through experience rather than instruction. The current report examined visuocortical response changes as human observers (N = 51, 19 male) learned, through differential classical conditioning, to associate specific screen locations with aversive outcomes. Using dense-array EEG and pupillometry, we tested the preregistered hypotheses of either sharpening or generalization around an aversively associated location following a single conditioning session. Competing hypotheses tested whether mean response changes would take the form of a Gaussian (generalization) or difference-of-Gaussian (sharpening) distribution over spatial positions, peaking at the viewing location paired with a noxious noise. Occipital 15 Hz steady-state visual evoked potential responses were selectively heightened when viewing aversively paired locations and displayed a nonlinear, difference-of-Gaussian profile across neighboring locations, consistent with suppressive surround modulation of nonprioritized positions. Measures of alpha-band (8-12 Hz) activity were differentially altered in anterior versus posterior locations, while pupil diameter exhibited selectively heightened responses to noise-paired locations but did not evince differences across the nonpaired locations. These results indicate that visuocortical spatial representations are sharpened in response to location-specific aversive conditioning, while top-down influences indexed by alpha-power reduction exhibit posterior generalization and anterior sharpening. |
Gerardo Fernández; Mario A. Parra Oculomotor behaviors and integrative memory functions in the Alzheimer's Clinical Syndrome Journal Article In: Journal of Alzheimer's Disease, vol. 82, no. 3, pp. 1033–1044, 2021. @article{Fernandez2021, Background: Biological information drawn from eye-tracking metrics is providing evidence regarding drivers of cognitive decline in Alzheimer's disease. In particular, pupil size has proved useful to investigate cognitive performance during online activities. Objective: To investigate the oculomotor correlates of impaired performance of patients with mild Alzheimer's Clinical Syndrome (ACS) on a recently developed memory paradigm, namely the Short-Term Memory Binding Test (STMBT). Methods: We assessed a sample of eighteen healthy controls (HC) and eighteen patients with a diagnosis of mild ACS with the STMBT while we recorded their oculomotor behaviors using pupillometry and eye-tracking. Results: As expected, a group (healthy controls versus ACS) by condition (Unbound Colours versus Bound Colours) interaction was found whereby behavioral group differences were paramount in the Bound Colours condition. Healthy controls' pupils dilated significantly more in the Bound Colours than in the Unbound Colours condition, a discrepancy not observed in ACS patients. Furthermore, ROC analysis revealed the abnormal pupil behaviors distinguished ACS patients from healthy controls with values of sensitivity and specify of 100%, thus outperforming both recognition scores and gaze duration. Conclusion: The biological correlates of Short-Term Memory Binding impairments appear to involve a network much wider than we have thought to date, which expands across cortical and subcortical structures. We discuss these findings focusing on their implications for our understanding of neurocognitive phenotypes in the preclinical stages of Alzheimer's disease and potential development of cognitive biomarkers that can support ongoing initiatives to prevent dementia. |
J. C. F. Winter; S. M. Petermeijer; L. Kooijman; D. Dodou Replicating five pupillometry studies of Eckhard Hess Journal Article In: International Journal of Psychophysiology, vol. 165, pp. 145–205, 2021. @article{Winter2021, Several papers by Eckhard Hess from the 1960s and 1970s report that the pupils dilate or constrict according to the interest value, arousing content, or mental demands of visual stimuli. However, Hess mostly used small sample sizes and undocumented luminance control. In a first experiment (N = 182) and a second preregistered experiment (N = 147), we replicated five studies of Hess using modern equipment. Our experiments (1) did not support the hypothesis of gender differences in pupil diameter change with respect to baseline (PC) when viewing stimuli of different interest value, (2) showed that solving more difficult multiplications yields a larger PC in the seconds before providing an answer and a larger maximum PC, but a smaller PC at a fixed time after the onset of the multiplication, (3) did not support the hypothesis that participants' PC mimics the pupil diameter in a pair of schematic eyes but not in single-eyed or three-eyed stimuli, (4) did not support the hypothesis of gender differences in PC when watching a video of a male trying to escape a mob, and (5) supported the hypothesis that arousing words yield a higher PC than non-arousing words. Although we did not observe consistent gender differences in PC, additional analyses showed gender differences in eye movements towards erogenous zones. Furthermore, PC strongly correlated with the luminance of the locations where participants looked. Overall, our replications confirm Hess's findings that pupils dilate in response to mental demands and stimuli of an arousing nature. Hess's hypotheses regarding pupil mimicry and gender differences in pupil dilation did not replicate. |
Kevin Silva Castanheira; Myle LoParco; A. Ross Otto Task-evoked pupillary responses track effort exertion: Evidence from task-switching Journal Article In: Cognitive, Affective and Behavioral Neuroscience, vol. 21, no. 3, pp. 592–606, 2021. @article{daSilvaCastanheira2021, A spate of research has examined how individuals regulate effortful processing in service of goal-directed behaviors. One key challenge in developing an account of this regulation is quantifying the momentary amount of cognitive effort exerted by an individual in service of their goals. A growing body of literature has suggested using task-evoked pupil dilations as a potential psychophysiological index of cognitive effort; however, it remains unclear whether pupil diameter indexes effort exertion or merely reflects task load, as both are tightly intertwined. Here, we attempt to disentangle these disparate accounts of pupil diameter by leveraging individual differences in executive function (as measured by Stroop interference) and a motivational manipulation (i.e., monetary incentives) while participants complete a task-switching paradigm. In line with both the effort and demand accounts, we observed larger task-evoked pupillary responses (TEPRs) for trials in which there was a task switch versus a task repetition. Additionally, we found that larger phasic pupillary responses at baseline (without reward incentives) predicted smaller switch costs. Mirroring this pattern, individual differences in reward-induced switch cost reductions were predicted by reward-induced increases in phasic pupil diameter. Finally, we observed that the interrelationship between effort and pupil diameter at baseline was modulated by individual differences in Stroop interference costs. Together, these findings provide support for an effort account of TEPRs, and suggest that pupillometry is a viable index of cognitive effort. |
Sarah Colby; Bob McMurray Cognitive and physiological measures of listening effort during degraded speech perception: Relating dual-task and pupillometry paradigms Journal Article In: Journal of Speech, Language, and Hearing Research, vol. 64, no. 9, pp. 3627–3652, 2021. @article{Colby2021, Purpose: Listening effort is quickly becoming an important metric for assessing speech perception in less-than-ideal situations. However, the relationship between the construct of listening effort and the measures used to assess it remains unclear. We compared two measures of listening effort: a cognitive dual task and a physiological pupillometry task. We sought to investigate the relationship between these measures of effort and whether engaging effort impacts speech accuracy. Method: In Experiment 1, 30 participants completed a dual task and a pupillometry task that were carefully matched in stimuli and design. The dual task consisted of a spoken word recognition task and a visual match-to-sample task. In the pupillometry task, pupil size was monitored while participants completed a spoken word recognition task. Both tasks presented words at three levels of listening difficulty (unmodified, eight-channel vocoding, and four-channel vocoding) and provided response feedback on every trial. We refined the pupillometry task in Experiment 2 (n = 31); crucially, participants no longer received response feedback. Finally, we ran a new group of subjects on both tasks in Experiment 3 (n = 30). Results: In Experiment 1, accuracy in the visual task decreased with increased signal degradation in the dual task, but pupil size was sensitive to accuracy and not vocoding condition. After removing feedback in Experiment 2, changes in pupil size were predicted by listening condition, suggesting the task was now sensitive to engaged effort. Both tasks were sensitive to listening difficulty in Experiment 3, but there was no relationship between the tasks and neither task predicted speech accuracy. Conclusions: Consistent with previous work, we found little evidence for a relationship between different measures of listening effort. We also found no evidence that effort predicts speech accuracy, suggesting that engaging more effort does not lead to improved speech recognition. Cognitive and physiological measures of listening effort are likely sensitive to different aspects of the construct of listening effort. |
Emily A. Burg; Tanvi Thakkar; Taylor Fields; Sara M. Misurelli; Stefanie E. Kuchinsky; Joseph Roche; Daniel J. Lee; Ruth Y. Litovsky Systematic comparison of trial exclusion criteria for pupillometry data analysis in individuals with single-sided deafness and normal hearing Journal Article In: Trends in Hearing, vol. 25, pp. 1–17, 2021. @article{Burg2021, The measurement of pupil dilation has become a common way to assess listening effort. Pupillometry data are subject to artifacts, requiring highly contaminated data to be discarded from analysis. It is unknown how trial exclusion criteria impact experimental results. The present study examined the effect of a common exclusion criterion, percentage of blinks, on speech intelligibility and pupil dilation measures in 9 participants with single-sided deafness (SSD) and 20 participants with normal hearing. Participants listened to and repeated sentences in quiet or with speech maskers. Pupillometry trials were processed using three levels of blink exclusion criteria: 15%, 30%, and 45%. These percentages reflect a threshold for missing data points in a trial, where trials that exceed the threshold are excluded from analysis. Results indicated that pupil dilation was significantly greater and intelligibility was significantly lower in the masker compared with the quiet condition for both groups. Across-group comparisons revealed that speech intelligibility in the SSD group decreased significantly more than the normal hearing group from quiet to masker conditions, but the change in pupil dilation was similar for both groups. There was no effect of blink criteria on speech intelligibility or pupil dilation results for either group. However, the total percentage of blinks in the masker condition was significantly greater than in the quiet condition for the SSD group, which is consistent with previous studies that have found a relationship between blinking and task difficulty. This association should be carefully considered in future experiments using pupillometry to gauge listening effort. |
Nicolai D. Ayasse; Alana J. Hodson; Arthur Wingfield The principle of least effort and comprehension of spoken sentences by younger and older adults Journal Article In: Frontiers in Psychology, vol. 12, pp. 629464, 2021. @article{Ayasse2021, There is considerable evidence that listeners' understanding of a spoken sentence need not always follow from a full analysis of the words and syntax of the utterance. Rather, listeners may instead conduct a superficial analysis, sampling some words and using presumed plausibility to arrive at an understanding of the sentence meaning. Because this latter strategy occurs more often for sentences with complex syntax that place a heavier processing burden on the listener than sentences with simpler syntax, shallow processing may represent a resource conserving strategy reflected in reduced processing effort. This factor may be even more important for older adults who as a group are known to have more limited working memory resources. In the present experiment, 40 older adults (Mage = 75.5 years) and 20 younger adults (Mage = 20.7) were tested for comprehension of plausible and implausible sentences with a simpler subject-relative embedded clause structure or a more complex object-relative embedded clause structure. Dilation of the pupil of the eye was recorded as an index of processing effort. Results confirmed greater comprehension accuracy for plausible than implausible sentences, and for sentences with simpler than more complex syntax, with both effects amplified for the older adults. Analysis of peak pupil dilations for implausible sentences revealed a complex three-way interaction between age, syntactic complexity, and plausibility. Results are discussed in terms of models of sentence comprehension, and pupillometry as an index of intentional task engagement. |
Naila Ayala; Ewa Niechwiej-Szwedo Effects of blocked vs. interleaved administration mode on saccade preparatory set revealed using pupillometry Journal Article In: Experimental Brain Research, vol. 239, no. 1, pp. 245–255, 2021. @article{Ayala2021a, Eye movements have been used extensively to assess information processing and cognitive function. However, significant variability in saccade performance has been observed, which could arise from methodological variations across different studies. For example, prosaccades and antisaccades have been studied using either a blocked or interleaved design, which has a significant influence on error rates and latency. This is problematic as it makes it difficult to compare saccade performance across studies and may limit the ability to use saccades as a behavioural assay to assess neurocognitive function. Thus, the current study examined how administration mode influences saccade related preparatory activity by employing pupil size as a non-invasive proxy for neural activity related to saccade planning and execution. Saccade performance and pupil dynamics were examined in eleven participants as they completed pro- and antisaccades in blocked and interleaved paradigms. Results showed that administration mode significantly modulated saccade performance and preparatory activity. Reaction times were longer for both pro- and antisaccades in the interleaved condition, compared to the blocked condition (p < 0.05). Prosaccade pupil dilations were larger in the interleaved condition (p < 0.05), while antisaccade pupil dilations did not significantly differ between administration modes. Additionally, ROC analysis provided preliminary evidence that pupil size can effectively predict saccade directional errors prior to saccade onset. We propose that task-evoked pupil dilations reflect an increase in preparatory activity for prosaccades and the corresponding cognitive demands associated with interleaved administration mode. Overall, the results highlight the importance that administration mode plays in the design of neurocognitive tasks. |
Naila Ayala; Matthew Heath Pupillometry reveals the role of arousal in a postexercise benefit to executive function Journal Article In: Brain Sciences, vol. 11, no. 8, pp. 1–10, 2021. @article{Ayala2021, A single bout of aerobic exercise improves executive function; however, the mechanism(s) underlying this improvement remains unclear. Here, we employed a 20-min bout of aerobic exercise, and at pre-and immediate post-exercise sessions examined executive function via pro-(i.e., saccade to veridical target location) and anti-saccade (i.e., saccade mirror symmetrical to a target) performance and pupillometry metrics. Notably, tonic and phasic pupillometry responses in oculomotor control provided a framework to determine the degree that arousal and/or executive resource recruitment influence behavior. Results demonstrated a pre-to post-exercise decrease in pro-and anti-saccade reaction times (p = 0.01) concurrent with a decrease and increase in tonic baseline pupil size and task-evoked pupil dilations, respectively (ps < 0.03). Such results demonstrate that an exercise-induced improvement in saccade performance is related to an executive-mediated “shift” in physiological and/or psychological arousal, supported by the locus coeruleus norepinephrine system to optimize task engagement. |
Thomas Armstrong; Sara Federman; Kari Hampson; Owen Crabtree; Bunmi O. Olatunji Fear learning in veterans with combat-related PTSD is linked to anxiety sensitivity: Evidence from self-report and pupillometry Journal Article In: Behavior Therapy, vol. 52, no. 1, pp. 149–161, 2021. @article{Armstrong2021, Several studies have observed heightened Pavlovian fear conditioning in PTSD. However, it is unclear how fear conditioning in PTSD is related to risk factors for the disorder, such as anxiety sensitivity. Fifty-one combat-exposed veterans (20 with PTSD, 31 without PTSD) completed a differential fear conditioning task in which one colored rectangle (CS +) predicted a loud scream (US), whereas a different colored rectangle (CS-) predicted no US. Veterans with PTSD were characterized by greater anxiety to the CS + but not the CS- during acquisition and extinction, and greater US expectancy during the CS + but not the CS- at extinction. Also, veterans with PTSD had greater pupil dilation to both CSs at extinction, but not at acquisition. Anxiety sensitivity was correlated with anxiety and US expectancy in response to the CS +, but not the CS-, at both acquisition and extinction, and also with pupil diameter to both the CS + and CS- at extinction. Nearly all of these relations held when covarying for PTSD symptoms and trait anxiety. These findings suggest that increased fear conditioning in PTSD may be related to elevated anxiety sensitivity. |
Sara Alhanbali; Kevin J. Munro; Piers Dawes; Peter J. Carolan; Rebecca E. Millman In: International Journal of Audiology, vol. 60, no. 10, pp. 762–772, 2021. @article{Alhanbali2021, Objective: Pupillometry is sensitive to cognitive resource allocation and has been used as a potential measure of listening-related effort and fatigue. We investigated associations between peak pupil diameter, pre-stimulus pupil diameter, performance on a listening task, and the dimensionality of self-reported outcomes (task-related listening effort and fatigue). Design: Pupillometry was recorded while participants performed a speech-in-noise task. Participants rated their experience of listening effort and fatigue using the NASA-Task Load Index (NASA-TLX) and the Visual Analogue Scale of Fatigue (VAS-F), respectively. The dimensionality of the NASA-TLX and the VAS-F was investigated using factor analysis. Study sample: 82 participants with either normal hearing or aided hearing impairment (age range: 55–85 years old, 43 male). Results: Hierarchal linear regression analyses suggested that pre-stimulus pupil diameter predicts a dimension of self-reported fatigue, which we interpreted as tiredness/drowsiness, and listening task performance when controlling for hearing level and age: Larger pre-stimulus pupil diameter was associated with less tiredness/drowsiness and better task performance. Conclusion: Pre-stimulus pupil diameter is a potential index of listening fatigue associated with speech processing in challenging listening conditions. To our knowledge, this is the first investigation of the associations between pre-stimulus pupil diameter and self-reported ratings of listening effort and fatigue. |
Serena K. Mon; Mira Nencheva; Francesca M. M. Citron; Casey Lew-Williams; Adele E. Goldberg Conventional metaphors elicit greater real-time engagement than literal paraphrases or concrete sentences Journal Article In: Journal of Memory and Language, vol. 121, pp. 104285, 2021. @article{Mon2021, Conventional metaphors (e.g., a firm grasp on an idea) are extremely common. A possible explanation for their ubiquity is that they are more engaging, evoking more focused attention, than their literal paraphrases (e.g., a good understanding of an idea). To evaluate whether, when, and why this may be true, we created a new database of 180 English sentences consisting of conventional metaphors, literal paraphrases, and concrete descriptions (e.g., a firm grip on a doorknob). Extensive norming matched differences across sentence types in complexity, plausibility, emotional valence, intensity, and familiarity of the key phrases. Then, using pupillometry to study the time course of metaphor processing, we predicted that metaphors would elicit greater event-evoked pupil dilation compared to other sentence types. Results confirmed the predicted increase beginning at the onset of the key phrase and lasting seconds beyond the end of the sentence. When metaphorical and literal sentences were compared directly in survey data, participants judged metaphorical sentences to convey “richer meaning,” but not more information. We conclude that conventional metaphors are more engaging than literal paraphrases or concrete sentences in a way that is irreducible to difficulty or ease, amount of information, short-term lexical access, or downstream inferences. |
Alice Milne; Sijia Zhao; Christina Tampakaki; Gabriela Bury; Maria Chait Sustained pupil responses are modulated by predictability of auditory sequences Journal Article In: Journal of Neuroscience, vol. 41, no. 28, pp. 6116–6127, 2021. @article{Milne2021, The brain is highly sensitive to auditory regularities and exploits the predictable order of sounds in many situations, from parsing complex auditory scenes, to the acquisition of language. To understand the impact of stimulus predictability on perception, it is important to determine how the detection of predictable structure influences processing and attention. Here we use pupillometry to gain insight into the effect of sensory regularity on arousal. Pupillometry is a commonly used measure of salience and processing effort, with more perceptually salient or perceptually demanding stimuli consistently associated with larger pupil diameters. In two experiments we tracked human listeners' pupil dynamics while they listened to sequences of 50ms tone pips of different frequencies. The order of the tone pips was either random, contained deterministic (fully predictable) regularities (experiment 1 |
2020 |
Lisa Wirz; Lars Schwabe Prioritized attentional processing: Acute stress, memory and stimulus emotionality facilitate attentional disengagement Journal Article In: Neuropsychologia, vol. 138, pp. 107334, 2020. @article{Wirz2020, Rapid attentional orienting toward relevant stimuli and efficient disengagement from irrelevant stimuli are critical for survival. Here, we examined the roles of memory processes, emotional arousal and acute stress in attentional disengagement. To this end, 64 healthy participants encoded negative and neutral facial expressions and, after being exposed to a stress or control manipulation, performed an attention task in which they had to disengage from these previously encoded as well as novel face stimuli. During the attention task, electroencephalography (EEG) and pupillometry data were recorded. Our results showed overall faster reaction times after acute stress and when participants had to disengage from emotionally negative or old facial expressions. Further, pupil dilations were larger in response to neutral faces. During disengagement, our EEG data revealed a reduced N2pc amplitude when participants disengaged from neutral compared to negative facial expressions when these were not presented before, as well as earlier onset latencies for the N400f (for disengagement from negative and old faces), the N2pc, and the LPP (for disengagement from negative faces). In addition, early visual processing of negative faces, as reflected in the P1 amplitude, was enhanced specifically in stressed participants. Our findings indicate that attentional disengagement is improved for negative and familiar stimuli and that stress facilitates not only attentional disengagement but also emotional processing in general. Together, these processes may represent important mechanisms enabling efficient performance and rapid threat detection. |
Nicole Wetzel; Wolfgang Einhäuser; Andreas Widmann Picture-evoked changes in pupil size predict learning success in children Journal Article In: Journal of Experimental Child Psychology, vol. 192, pp. 1–18, 2020. @article{Wetzel2020, Episodic memory, the ability to remember past events in time and place, develops during childhood. Much knowledge about the underlying neuronal mechanisms has been gained from methods not suitable for children. We applied pupillometry to study memory encoding and recognition mechanisms. Children aged 8 and 9 years (n = 24) and adults (n = 24) studied a set of visual scenes to later distinguish them from new pictures. Children performed worse than adults, demonstrating immature episodic memory. During memorization, picture-related changes in pupil diameter predicted later successful recognition. This prediction effect was also observed on a single-trial level. During retrieval, novel pictures showed stronger pupil constriction than familiar pictures in both age groups. The statistically independent effects of objective familiarity (previously presented pictures) versus subjective familiarity (pictures evaluated as familiar independent of the prior presentation) suggest dissociable underlying brain mechanisms. In addition, we isolated principal components of the picture-related pupil response that were differently affected by the memorization and retrieval effects. Results are discussed in the context of the maturation of the medial temporal lobe and prefrontal networks. Our results demonstrate the dissociation of distinct contributions to episodic memory with a psychophysiological method that is suitable for a wide age spectrum. |
Max Schneider; Immanuel G. Elbau; Teachawidd Nantawisarakul; Dorothee Pöhlchen; Tanja Brückl; Michael Czisch; Philipp G. Saemann; Michael D. Lee; Elisabeth B. Binder; Victor I. Spoormaker Pupil dilation during reward anticipation is correlated to depressive symptom load in patients with major depressive disorder Journal Article In: Brain Sciences, vol. 10, no. 12, pp. 1–15, 2020. @article{Schneider2020a, Depression is a debilitating disorder with high prevalence and socioeconomic cost, but the brain-physiological processes that are altered during depressive states are not well understood. Here, we build on recent findings in macaques that indicate a direct causal relationship between pupil dilation and anterior cingulate cortex mediated arousal during anticipation of reward. We translated these findings to human subjects with concomitant pupillometry/fMRI in a sample of unmedicated participants diagnosed with major depression and healthy controls. We could show that the upregulation and maintenance of arousal in anticipation of reward was disrupted in patients in a symptom-load dependent manner. We could further show that the failure to maintain reward anticipatory arousal showed state-marker properties, as it tracked the load and impact of depressive symptoms independent of prior diagnosis status. Further, group differences of anticipatory arousal and continuous correlations with symptom load were not traceable only at the level of pupillometric responses, but were mirrored also at the neural level within salience network hubs. The upregulation and maintenance of arousal during reward anticipation is a novel translational and well-traceable process that could prove a promising gateway to a physiologically informed patient stratification and targeted interventions. |
Daniel J. Schad; Michael A. Rapp; Maria Garbusow; Stephan Nebe; Miriam Sebold; Elisabeth Obst; Christian Sommer; Lorenz Deserno; Milena Rabovsky; Eva Friedel; Nina Romanczuk-Seiferth; Hans Ulrich Wittchen; Ulrich S. Zimmermann; Henrik Walter; Philipp Sterzer; Michael N. Smolka; Florian Schlagenhauf; Andreas Heinz; Peter Dayan; Quentin J. M. M. Huys Dissociating neural learning signals in human sign- and goal-trackers Journal Article In: Nature Human Behaviour, vol. 4, no. 2, pp. 201–214, 2020. @article{Schad2020, Individuals differ in how they learn from experience. In Pavlovian conditioning models, where cues predict reinforcer delivery at a different goal location, some animals—called sign-trackers—come to approach the cue, whereas others, called goal-trackers, approach the goal. In sign-trackers, model-free phasic dopaminergic reward-prediction errors underlie learning, which renders stimuli ‘wanted'. Goal-trackers do not rely on dopamine for learning and are thought to use model-based learning. We demonstrate this double dissociation in 129 male humans using eye-tracking, pupillometry and functional magnetic resonance imaging informed by computational models of sign- and goal-tracking. We show that sign-trackers exhibit a neural reward prediction error signal that is not detectable in goal-trackers. Model-free value only guides gaze and pupil dilation in sign-trackers. Goal-trackers instead exhibit a stronger model-based neural state prediction error signal. This model-based construct determines gaze and pupil dilation more in goal-trackers. |
Jamie Reilly; Bonnie Zuckerman; Alexandra Kelly; Maurice Flurie; Sagar Rao Neuromodulation of cursing in American English: A combined tDCS and pupillometry study Journal Article In: Brain and Language, vol. 206, pp. 1–8, 2020. @article{Reilly2020, Many neurological disorders are associated with excessive and/or uncontrolled cursing. The right prefrontal cortex has long been implicated in a diverse range of cognitive processes that underlie the propensity for cursing, including non-propositional language representation, emotion regulation, theory of mind, and affective arousal. Neurogenic cursing often poses significant negative social consequences, and there is no known behavioral intervention for this communicative disorder. We examined whether right vs. left lateralized prefrontal neurostimultion via tDCS could modulate taboo word production in neurotypical adults. We employed a pre/post design with a bilateral frontal electrode montage. Half the participants received left anodal and right cathodal stimulation; the remainder received the opposite polarity stimulation at the same anatomical loci. We employed physiological (pupillometry) and behavioral (reaction time) dependent measures as participants read aloud taboo and non-taboo words. Pupillary responses demonstrated a crossover reaction, suggestive of modulation of phasic arousal during cursing. Participants in the right anodal condition showed elevated pupil responses for taboo words post stimulation. In contrast, participants in the right cathodal condition showed relative dampening of pupil responses for taboo words post stimulation. We observed no effects of stimulation on response times. We interpret these findings as supporting modulation of right hemisphere affective arousal that disproportionately impacts taboo word processing. We discuss alternate accounts of the data and future applications to neurological disorders. |
Antonella Pomè; Paola Binda; Guido Marco Cicchini; David C. Burr Pupillometry correlates of visual priming, and their dependency on autistic traits Journal Article In: Journal of Vision, vol. 20, no. 3, pp. 1–12, 2020. @article{Pome2020, In paradigms of visual search where the search feature (say color) can change from trial to trials, responses are faster for trials where the search color is repeated than when it changes. This is a clear example of "priming" of attention. Here we test whether the priming effects can be revealed by pupillometry, and also whether they are related to autistic-like personality traits, as measured by the Autism-Spectrum Quotient (AQ). We repeated Maljkovic and Nakayama's (1994) classic priming experiment, asking subjects to identify rapidly the shape of a singleton target defined by color. As expected, reaction times were faster when target color repeated, and the effect accumulated over several trials; but the magnitude of the effect did not correlate with AQ. Reaction times were also faster when target position was repeated, again independent of AQ. Presentation of stimuli caused the pupil to dilate, and the magnitude of dilation was greater for switched than repeated trials. This effect did not accumulate over trials, and did not correlate with the reaction times difference, suggesting that the two indexes measure independent aspects of the priming phenomenon. Importantly, the amplitude of pupil modulation correlated negatively with AQ, and was significant only for those participants with low AQ. The results confirm that pupillometry can track perceptual and attentional processes, and furnish useful information unobtainable from standard psychophysics, including interesting dependencies on personality traits. |
Dorothee Pöhlchen; Laura Leuchs; Florian P. Binder; Borbala Blaskovich; Taechawidd Nantawisarakul; Pavlos Topalidis; Tanja M. Brückl; Seth D. Norrholm; Tanja Jovanovic; Victor I. Spoormaker; Elisabeth B. Binder; Michael Czisch; Angelika Erhardt; Norma C. Grandi; Sanja Ilic-Cocic; Susanne Lucae; Philipp Sämann; Alina Tontsch No robust differences in fear conditioning between patients with fear-related disorders and healthy controls Journal Article In: Behaviour Research and Therapy, vol. 129, pp. 1–10, 2020. @article{Poehlchen2020, Fear conditioning and extinction serve as a dominant model for the development and maintenance of pathological anxiety, particularly for phasic fear to specific stimuli or situations. The validity of this model would be supported by differences in the physiological or subjective fear response between patients with fear-related disorders and healthy controls, whereas the model's validity would be questioned by a lack of such differences. We derived pupillometry, skin conductance response and startle electromyography as well as unconditioned stimulus expectancy in a two-day fear acquisition, immediate extinction and recall task and compared an unmedicated group of patients (n = 73) with phobias or panic disorder and a group of patients with posttraumatic stress disorder (PTSD |
Nick B. Pandža; Ian Phillips; Valerie P. Karuzis; Polly O'Rourke; Stefanie E. Kuchinsky Neurostimulation and pupillometry: New directions for learning and research in applied linguistics Journal Article In: Annual Review of Applied Linguistics, vol. 40, pp. 56–77, 2020. @article{Pandza2020, This paper begins by discussing new trends in the use of neurostimulation techniques in cognitive science and learning research, as well as the nascent research on their application in second language learning. To illustrate this, an experiment designed to investigate the impact of transcutaneous vagus nerve stimulation (tVNS), which is delivered via earbuds, on how learners process and learn Mandarin tones is reported. Pupillometry, which is an index of cognitive effort, is explained and illustrated as one way to assess the impact of tVNS. Participants in the study were native English speakers, naïve to tone languages, pseudorandomly assigned to active or control conditions, while balancing for nonlinguistic pitch ability and musical experience. Their performance after tVNS was assessed using a range of more traditional language outcome measures, including accuracy and reaction times from lexical recognition and recall tasks and was triangulated with pupillometry during word-learning to help understand the mechanism through which tVNS operates. Findings are discussed in light of the literatures on lexical tone learning, cognitive effort, and neurostimulation, including specific benefits for learners of tone languages. Recommendations are made for future work on the increasingly popular area of neurostimulation for the field of applied linguistics in the 40th anniversary issue of ARAL. |
Drew J. McLaughlin; Kristin J. Van Engen Task-evoked pupil response for accurately recognized accented speech Journal Article In: The Journal of the Acoustical Society of America, vol. 147, no. 2, pp. EL151–EL156, 2020. @article{McLaughlin2020, Unfamiliar second-language (L2) accents present a common challenge to speech understanding. However, the extent to which accurately recognized unfamiliar L2-accented speech imposes a greater cognitive load than native speech remains unclear. The current study used pupillometry to assess cognitive load for native English listeners during the per- ception of intelligible Mandarin Chinese-accented English and American-accented English. Results showed greater pupil response (indicating greater cognitive load) for the unfamiliar L2-accented speech. These findings indicate that the mismatches between unfamiliar L2- accented speech and native listeners' linguistic representations impose greater cognitive load even when recognition accuracy is at ceiling. |
Kevin P. Madore; Anna M. Khazenzon; Cameron W. Backes; Jiefeng Jiang; Melina R. Uncapher; Anthony M. Norcia; Anthony D. Wagner Memory failure predicted by attention lapsing and media multitasking Journal Article In: Nature, vol. 587, no. 7832, pp. 87–91, 2020. @article{Madore2020, With the explosion of digital media and technologies, scholars, educators and the public have become increasingly vocal about the role that an ‘attention economy' has in our lives1. The rise of the current digital culture coincides with longstanding scientific questions about why humans sometimes remember and sometimes forget, and why some individuals remember better than others2–6. Here we examine whether spontaneous attention lapses—in the moment7–12, across individuals13–15 and as a function of everyday media multitasking16–19—negatively correlate with remembering. Electroencephalography and pupillometry measures of attention20,21 were recorded as eighty young adults (mean age, 21.7 years) performed a goal-directed episodic encoding and retrieval task22. Trait-level sustained attention was further quantified using task-based23 and questionnaire measures24,25. Using trial-to-trial retrieval data, we show that tonic lapses in attention in the moment before remembering, assayed by posterior alpha power and pupil diameter, were correlated with reductions in neural signals of goal coding and memory, along with behavioural forgetting. Independent measures of trait-level attention lapsing mediated the relationship between neural assays of lapsing and memory performance, and between media multitasking and memory. Attention lapses partially account for why we remember or forget in the moment, and why some individuals remember better than others. Heavier media multitasking is associated with a propensity to have attention lapses and forget. |
Russell A. Cohen Hoffing; Nina Lauharatanahirun; Daniel E. Forster; Javier O. Garcia; Jean M. Vettel; Steven M. Thurman Dissociable mappings of tonic and phasic pupillary features onto cognitive processes involved in mental arithmetic Journal Article In: PLoS ONE, vol. 15, no. 3, pp. e0230517, 2020. @article{Hoffing2020, Pupil size modulations have been used for decades as a window into the mind, and several pupillary features have been implicated in a variety of cognitive processes. Thus, a general challenge facing the field of pupillometry has been understanding which pupil features should be most relevant for explaining behavior in a given task domain. In the present study, a longitudinal design was employed where participants completed 8 biweekly sessions of a classic mental arithmetic task for the purposes of teasing apart the relationships between tonic/phasic pupil features (baseline, peak amplitude, peak latency) and two task-related cognitive processes including mental processing load (indexed by math question difficulty) and decision making (indexed by response times). We used multi-level modeling to account for individual variation while identifying pupil-to-behavior relationships at the single-trial and between-session levels. We show a dissociation between phasic and tonic features with peak amplitude and latency (but not baseline) driven by ongoing task-related processing, whereas baseline was driven by state-level effects that changed over a longer time period (i.e. weeks). Finally, we report a dissociation between peak amplitude and latency whereby amplitude reflected surprise and processing load, and latency reflected decision making times. |
Eugen Fischer; Paul E. Engelhardt Lingering stereotypes: Salience bias in philosophical argument Journal Article In: Mind and Language, vol. 35, no. 4, pp. 415–439, 2020. @article{Fischer2020, Many philosophical thought experiments and arguments involve unusual cases. We present empirical reasons to doubt the reliability of intuitive judgments and conclusions about such cases. Inferences and intuitions prompted by verbal case descriptions are influenced by routine comprehension processes which invoke stereotypes. We build on psycholinguistic findings to determine conditions under which the stereotype associated with the most salient sense of a word predictably supports inappropriate inferences from descriptions of unusual (stereotype-divergent) cases. We conduct an experiment that combines plausibility ratings with pupillometry to document this “salience bias.” We find that under certain conditions, competent speakers automatically make stereotypical inferences they know to be inappropriate. |
Mojgan Farahani; Vijay Parsa; Björn Herrmann; Mason Kadem; Ingrid Johnsrude; Philip C. Doyle An auditory-perceptual and pupillometric study of vocal strain and listening effort in adductor spasmodic dysphonia Journal Article In: Applied Sciences, vol. 10, no. 17, pp. 5907, 2020. @article{Farahani2020, This study evaluated ratings of vocal strain and perceived listening effort by normal hearing participants while listening to speech samples produced by talkers with adductor spasmodic dysphonia (AdSD). In addition, objective listening effort was measured through concurrent pupillometry to determine whether listening to disordered voices changed arousal as a result of emotional state or cognitive load. Recordings of the second sentence of the "Rainbow Passage" produced by talkers with varying degrees of AdSD served as speech stimuli. Twenty naïve young adult listeners perceptually evaluated these stimuli on the dimensions of vocal strain and listening effort using two separate visual analogue scales. While making the auditory-perceptual judgments, listeners' pupil characteristics were objectively measured in synchrony with the presentation of each voice stimulus. Data analyses revealed moderate-to-high inter- and intra-rater reliability. A significant positive correlation was found between the ratings of vocal strain and listening effort. In addition, listeners displayed greater peak pupil dilation (PPD) when listening to more strained and effortful voice samples. Findings from this study suggest that when combined with an auditory-perceptual task, non-volitional physiologic changes in pupil response may serve as an indicator of listening and cognitive effort or arousal. |
Camilla E. J. Elphick; Graham E. Pike; Graham J. Hole You can believe your eyes: Measuring implicit recognition in a lineup with pupillometry Journal Article In: Psychology, Crime and Law, vol. 26, no. 1, pp. 67–92, 2020. @article{Elphick2020, As pupil size is affected by cognitive processes, we investigated whether it could serve as an independent indicator of target recognition in lineups. Participants saw a simulated crime video, followed by two viewings of either a target-present or target-absent video lineup while pupil size was measured with an eye-tracker. Participants who made correct identifications showed significantly larger pupil sizes when viewing the target compared with distractors. Some participants were uncertain about their choice of face from the lineup, but nevertheless showed pupillary changes when viewing the target, suggesting covert recognition of the target face had occurred. The results suggest that pupillometry might be a useful aid in assessing the accuracy of an eyewitness' identification. |
Daniel S. Drew; Kinan Muhammed; Fahd Baig; Mark Kelly; Youssuf Saleh; Nagaraja Sarangmat; David Okai; Michele Hu; Sanjay Manohar; Masud Husain Dopamine and reward hypersensitivity in Parkinson's disease with impulse control disorder Journal Article In: Brain, vol. 143, no. 8, pp. 2502–2518, 2020. @article{Drew2020, Impulse control disorders in Parkinson's disease are common neuropsychiatric complications associated with dopamine replacement therapy. Some patients treated with dopamine agonists develop pathological behaviours, such as gambling, compulsive eating, shopping, or disinhibited sexual behaviours, which can have a severe impact on their lives and that of their families. In this study we investigated whether hypersensitivity to reward might contribute to these pathological behaviours and how this is influenced by dopaminergic medication. We asked participants to shift their gaze to a visual target as quickly as possible, in order to obtain reward. Critically, the reward incentive on offer varied over trials. Motivational effects were indexed by pupillometry and saccadic velocity, and patients were tested ON and OFF dopaminergic medication, allowing us to measure the effect of dopaminergic medication changes on reward sensitivity. Twenty-three Parkinson's disease patients with a history of impulse control disorders were compared to 26 patients without such behaviours, and 31 elderly healthy controls. Intriguingly, behavioural apathy was reported alongside impulsivity in the majority of patients with impulse control disorders. Individuals with impulse control disorders also exhibited heightened sensitivity to exogenous monetary rewards cues both ON and OFF (overnight withdrawal) dopamine medication, as indexed by pupillary dilation in anticipation of reward. Being OFF dopaminergic medication overnight did not modulate pupillary reward sensitivity in impulse control disorder patients, whereas in control patients reward sensitivity was significantly reduced when OFF dopamine. These effects were independent of cognitive impairment or total levodopa equivalent dose. Although dopamine agonist dose did modulate pupillary responses to reward, the pattern of results was replicated even when patients with impulse control disorders on dopamine agonists were excluded from the analysis. The findings suggest that hypersensitivity to rewards might be a contributing factor to the development of impulse control disorders in Parkinson's disease. However, there was no difference in reward sensitivity between patient groups when ON dopamine medication, suggesting that impulse control disorders may not emerge simply because of a direct effect of dopaminergic drug level on reward sensitivity. The pupillary reward sensitivity measure described here provides a means to differentiate, using a physiological measure, Parkinson's disease patients with impulse control disorder from those who do not experience such symptoms. Moreover, follow-up of control patients indicated that increased pupillary modulation by reward can be predictive of the risk of future emergence of impulse control disorders and may thereby provide the potential for early identification of patients who are more likely to develop these symptoms. |
Violet A. Brown; Drew J. McLaughlin; Julia F. Strand; Kristin J. Van Engen Rapid adaptation to fully intelligible nonnative-accented speech reduces listening effort Journal Article In: Quarterly Journal of Experimental Psychology, vol. 73, no. 9, pp. 1431–1443, 2020. @article{Brown2020b, In noisy settings or when listening to an unfamiliar talker or accent, it can be difficult to understand spoken language. This difficulty typically results in reductions in speech intelligibility, but may also increase the effort necessary to process the speech even when intelligibility is unaffected. In this study, we used a dual-task paradigm and pupillometry to assess the cognitive costs associated with processing fully intelligible accented speech, predicting that rapid perceptual adaptation to an accent would result in decreased listening effort over time. The behavioural and physiological paradigms provided converging evidence that listeners expend greater effort when processing nonnative- relative to native-accented speech, and both experiments also revealed an overall reduction in listening effort over the course of the experiment. Only the pupillometry experiment, however, revealed greater adaptation to nonnative- relative to native-accented speech. An exploratory analysis of the dual-task data that attempted to minimise practice effects revealed weak evidence for greater adaptation to the nonnative accent. These results suggest that even when speech is fully intelligible, resolving deviations between the acoustic input and stored lexical representations incurs a processing cost, and adaptation may attenuate this cost. |
Giulia Borghini; Valerie Hazan Effects of acoustic and semantic cues on listening effort during native and non-native speech perception Journal Article In: The Journal of the Acoustical Society of America, vol. 147, no. 6, pp. 3783–3794, 2020. @article{Borghini2020, Relative to native listeners, non-native listeners who are immersed in a second language environment experience increased listening effort and reduced ability to successfully perform an additional task while listening. Previous research demonstrated that listeners can exploit a variety of intelligibility-enhancing cues to cope with adverse listening conditions. However, little is known about the implications of those speech perception strategies for listening effort. The current research aims to investigate by means of pupillometry how listening effort is modulated in native and non-native listeners by the availability of semantic context and acoustic enhancements during the comprehension of spoken sentences. For this purpose, semantic plausibility and speaking style were manipulated both separately and in combination during a speech perception task in noise. The signal to noise ratio was individually adjusted for each participant in order to target 50% intelligibility level. Behavioural results indicated that native and non-native listeners were equally able to fruitfully exploit both semantic and acoustic cues to aid their comprehension. Pupil data indicated that listening effort was reduced for both groups of listeners when acoustic enhancements were available, while the presence of a plausible semantic context did not lead to a reduction in listening effort. |
Naila Ayala; Matthew Heath Executive dysfunction after a sport-related concussion is independent of task-based symptom burden Journal Article In: Journal of Neurotrauma, vol. 37, pp. 2558–2568, 2020. @article{Ayala2020, A sport-related concussion (SRC) results in short- and long-term deficits in oculomotor control; however, it is unclear whether this change reflects executive dysfunction and/or a performance decrement due to an increase in task-based symptom burden. Here, individuals with a SRC - and age- and sex-matched controls - completed an antisaccade task (i.e., saccade mirror-symmetrical to a target) during the early (initial assessment: <=12 days) and later (follow-up assessment: < 30 days) stages of recovery. Antisaccades were used because they require top-down executive control and exhibit performance decrements following a SRC. Reaction time (RT) and directional errors were included with pupillometry because pupil size in the antisaccade task has been shown to provide a neural proxy for executive control. In addition, the Sport-Concussion Assessment Tool (SCAT-5) symptom checklist was completed prior to and after each oculomotor assessment to identify a possible task-based increase in symptomology. The SRC group yielded longer initial assessment RTs, more directional errors and larger task-evoked pupil dilations (TEPD) than the control group. At the follow-up assessment, RTs for the SRC and control group did not reliably differ; however, the former demonstrated more directional errors and larger TEPDs. SCAT-5 symptom severity scores did not vary from the pre- to post-oculomotor evaluation for either initial or follow-up assessments. Accordingly, a SRC imparts a persistent executive dysfunction to oculomotor planning independent of a task-based increase in symptom burden. These findings evince that antisaccades serve as an effective tool to identify subtle executive deficits during the early and later stages of SRC recovery. |
Satoshi Nakakoga; Hiroshi Higashi; Junya Muramatsu; Shigeki Nakauchi; Tetsuto Minami Asymmetrical characteristics of emotional responses to pictures and sounds: Evidence from pupillometry Journal Article In: PLoS ONE, vol. 15, no. 4, pp. e0230775, 2020. @article{Nakakoga2020, In daily life, our emotions are often elicited by a multimodal environment, mainly visual and auditory stimuli. Therefore, it is crucial to investigate the symmetrical characteristics of emotional responses to pictures and sounds. In this study, we aimed to elucidate the relationship of attentional states to emotional unimodal stimuli (pictures or sounds) and emotional responses by measuring the pupil diameter, which reflects the emotional arousal associated with increased sympathetic activity. Our hypothesis was that the emotional responses to both the image and sound stimuli are symmetrical: emotion might be suppressed when attentional resources are allocated to another stimulus of the same modality as the emotional stimulus-such as a dot presented at the same time as an emotional image, and a beep sound presented at the same time as an emotional sound. In our two experiments, data for 24 participants were analyzed for a pupillary response. In experiment 1, we investigated the relationship of the attentional state with emotional visual stimuli (International Affective Picture System) and emotional responses by using pupillometry. We set four task conditions to modulate the attentional state (emotional task, no task, visual detection task, and auditory detection task). We observed that the velocity of pupillary dilation was faster during the presentation of emotionally arousing pictures compared to that of neutral ones, regardless of the valence of the pictures. Importantly, this effect was not dependent on the task condition. In experiment 2, we investigated the relationship of the attentional state with emotional auditory sounds (International Affective Digitized Sounds) and emotional responses. We observed a trend towards a significant interaction between the stimulus and the task conditions with regard to the velocity of pupillary dilation. In the emotional and auditory detection tasks, the velocity of pupillary dilation was faster with positive and neutral sounds than negative sounds. However, there were no significant differences between the no task and visual detection task conditions. Taken together, the current data reveal that different pupillary responses were elicited to emotional visual and auditory stimuli, at least in the point that there is no attentional effect to emotional responses to visual stimuli, despite both experiments being sufficiently controlled to be of symmetrical experimental design. |
2019 |
Felicia Zhang; Sagi Jaffe-Dax; Robert C. Wilson; Lauren L. Emberson Prediction in infants and adults: A pupillometry study Journal Article In: Developmental Science, vol. 22, no. 4, pp. 1–9, 2019. @article{Zhang2019h, Adults use both bottom-up sensory inputs and top-down signals to generate predictions about future sensory inputs. Infants have also been shown to make predictions with simple stimuli and recent work has suggested top-down processing is available early in infancy. However, it is unknown whether this indicates that top-down prediction is an ability that is continuous across the lifespan or whether an infant's ability to predict is different from an adult's, qualitatively or quantitatively. We employed pupillometry to provide a direct comparison of prediction abilities across these disparate age groups. Pupil dilation response (PDR) was measured in 6-month olds and adults as they completed an identical implicit learning task designed to help learn associations between sounds and pictures. We found significantly larger PDR for visual omission trials (i.e. trials that violated participants' predictions without the presentation of new stimuli to control for bottom-up signals) compared to visual present trials (i.e. trials that confirmed participants' predictions) in both age groups. Furthermore, a computational learning model that is closely linked to prediction error (Rescorla-Wagner model) demonstrated similar learning trajectories suggesting a continuity of predictive capacity and learning across the two age groups. |
Peter Vincent; Thomas Parr; David Benrimoh; Karl J. Friston With an eye on uncertainty: Modelling pupillary responses to environmental volatility Journal Article In: PLOS Computational Biology, vol. 15, no. 7, pp. e1007126, 2019. @article{Vincent2019, Living creatures must accurately infer the nature of their environments. They do this despite being confronted by stochastic and context sensitive contingencies—and so must constantly update their beliefs regarding their uncertainty about what might come next. In this work, we examine how we deal with uncertainty that evolves over time. This prospective uncertainty (or imprecision) is referred to as volatility and has previously been linked to noradrenergic signals that originate in the locus coeruleus. Using pupillary dilatation as a measure of central noradrenergic signalling, we tested the hypothesis that changes in pupil diameter reflect inferences humans make about environmental volatility. To do so, we collected pupillometry data from participants presented with a stream of numbers. We generated these numbers from a process with varying degrees of volatility. By measuring pupillary dilatation in response to these stimuli—and simulating the inferences made by an ideal Bayesian observer of the same stimuli—we demonstrate that humans update their beliefs about environmental contingencies in a Bayes optimal way. We show this by comparing general linear (convolution) models that formalised competing hypotheses about the causes of pupillary changes. We found greater evidence for models that included Bayes optimal estimates of volatility than those without. We additionally explore the interaction between different causes of pupil dilation and suggest a quantitative approach to characterising a person's prior beliefs about volatility. |
Megan H. Papesh; Juan D. Guevara Pinto Spotting rare items makes the brain “blink” harder: Evidence from pupillometry Journal Article In: Attention, Perception, and Psychophysics, vol. 81, no. 8, pp. 2635–2647, 2019. @article{Papesh2019, In many visual search tasks (e.g., cancer screening, airport baggage inspections), the most serious search targets occur infrequently. As an ironic side effect, when observers finally encounter important objects (e.g., a weapon in baggage), they often fail to notice them, a phenomenon known as the low-prevalence effect (LPE). Although many studies have investigated LPE search errors, we investigated the attentional consequences of successful rare target detection. Using an attentional blink paradigm, we manipulated how often observers encountered the first serial target (T1), then measured its effects on their ability to detect a following target (T2). Across two experiments, we show that the LPE is more than just an inflated miss rate: When observers successfully detected rare targets, they were less likely to spot subsequent targets. Using pupillometry to index locus-coeruleus (LC) mediated attentional engagement, Experiment 2 confirmed that an LC refractory period mediates the attentional blink (`Nieuwenhuis, Gilzenrat, Holmes, & Cohen, 2005, Journal of Experimental Psychology: General, 134[3], 291–307), and that these effects emerge relatively quickly following T1 onset. Moreover, in both behavioral and pupil analyses, we found that detecting low-prevalence targets exacerbates the LC refractory period. Consequences for theories of the LPE are discussed. |
Sijia Zhao; Gabriela Bury; Alice Milne; Maria Chait Pupillometry as an objective measure of sustained attention in young and older listeners Journal Article In: Trends in Hearing, vol. 23, pp. 1–21, 2019. @article{Zhao2019a, The ability to sustain attention on a task-relevant sound-source whilst avoiding distraction from other concurrent sounds is fundamental to listening in crowded environments. To isolate this aspect of hearing we designed a paradigm that continuously measured behavioural and pupillometry responses during 25-second-long trials in young (18-35 yo) and older (63-79 yo) participants. The auditory stimuli consisted of a number (1, 2 or 3) of concurrent, spectrally distinct tone streams. On each trial, participants detected brief silent gaps in one of the streams whilst resisting distraction from the others. Behavioural performance demonstrated increasing difficulty with time-on-task and with number/proximity of distractor streams. In young listeners (N=20), pupillometry revealed that pupil diameter (on the group and individual level) was dynamically modulated by instantaneous task difficulty such that periods where behavioural performance revealed a strain on sustained attention, were also accompanied by increased pupil diameter. Only trials on which participants performed successfully were included in the pupillometry analysis. Therefore, the observed effects reflect consequences of task demands as opposed to failure to attend.In line with existing reports, we observed global changes to pupil dynamics in the older group, including decreased pupil diameter, a limited dilation range, and reduced temporal variability. However, despite these changes, the older group showed similar effects of attentive tracking to those observed in the younger listeners. Overall, our results demonstrate that pupillometry can be a reliable and time-sensitive measure of the effort associated with attentive tracking over long durations in both young and (with some caveats) older listeners. |
Felicia Zhang; Lauren L. Emberson Opposing timing constraints severely limit the use of pupillometry to investigate visual statistical learning Journal Article In: Frontiers in Psychology, vol. 10, pp. 1792, 2019. @article{Zhang2019c, Majority of visual statistical learning (VSL) research uses only offline measures, collected after the familiarization phase (i.e. learning) has occurred. Offline measures have revealed a lot about the extent of statistical learning (SL) but less is known about the learning mechanisms that support VSL. Studies have shown that prediction can be a potential learning mechanism for VSL, but it is difficult to examine the role of prediction in VSL using offline measures alone. Pupil diameter is a promising online measure to index prediction in VSL because it can be collected during learning, requires no overt action or task and can be used in a wide-range of populations (e.g., infants and adults). Furthermore, pupil diameter has already been used to investigate processes that are part of prediction such as prediction error and updating. While the properties of pupil diameter have the potentially to powerfully expand studies in VSL, through a series of three experiments, we find that the two are not compatible with each other. Our results revealed that pupil diameter, used to index prediction, is not related to offline measures of learning. We also found that pupil differences that appear to be a result of prediction, are actually a result of where we chose to baseline instead. Ultimately, we conclude that the fast-paced nature of VSL paradigms make it incompatible with the slow nature of pupil change. Therefore, our findings suggest pupillometry should not be used to investigate learning mechanisms in fast-paced VSL tasks. |
Chad C. Williams; Mitchel Kappen; Cameron D. Hassall; Bruce Wright; Olave E. Krigolson Thinking theta and alpha: Mechanisms of intuitive and analytical reasoning Journal Article In: NeuroImage, vol. 189, pp. 574–580, 2019. @article{Williams2019, Humans have a unique ability to engage in different modes of thinking. Intuitive thinking (coined System 1, see Kahneman, 2011) is fast, automatic, and effortless whereas analytical thinking (coined System 2) is slow, contemplative, and effortful. We extend seminal pupillometry research examining these modes of thinking by using electroencephalography (EEG) to decipher their respective underlying neural mechanisms. We demonstrate that System 1 thinking is characterized by an increase in parietal alpha EEG power reflecting autonomic access to long-term memory and a release of attentional resources whereas System 2 thinking is characterized by an increase in frontal theta EEG power indicative of the engagement of cognitive control and working memory processes. Consider our results in terms of an example - a child may need cognitive control and working memory when contemplating a mathematics problem yet an adullt can drive a car with little to no attention by drawing on easily accessed memories. Importantly, the unravelling of intuitive and analytical thinking mechanisms and their neural signatures will provide insight as to how different modes of thinking drive our everyday lives. |
Leonhard Waschke; Sarah Tune; Jonas Obleser Local cortical desynchronization and pupil-linked arousal differentially shape brain states for optimal sensory performance Journal Article In: eLife, vol. 8, pp. 1–27, 2019. @article{Waschke2019, Instantaneous brain states have consequences for our sensation, perception, and behaviour. Fluctuations in arousal and neural desynchronization likely pose perceptually relevant states. However, their relationship and their relative impact on perception is unclear. We here show that, at the single-trial level in humans, local desynchronization in sensory cortex (expressed as time-series entropy) versus pupil- linked arousal differentially impact perceptual processing. While we recorded electroencephalography (EEG) and pupillometry data, stimuli of a demanding auditory discrimination task were presented into states of high or low desynchronization of auditory cortex via a real-time closed-loop setup. Desynchronization and arousal distinctly influenced stimulus-evoked activity and shaped behaviour displaying an inverted u-shaped relationship: States of intermediate desynchronization elicited minimal response bias and fastest responses, while states of intermediate arousal gave rise to highest response sensitivity. Our results speak to a model in which independent states of local desynchronization and global arousal jointly optimise sensory processing and performance. |
Amy T. Walsh; David Carmel; Gina M. Grimshaw Reward elicits cognitive control over emotional distraction: Evidence from pupillometry Journal Article In: Cognitive, Affective and Behavioral Neuroscience, vol. 19, no. 3, pp. 537–554, 2019. @article{Walsh2019, Attention is biased toward emotional stimuli, even when they are irrelevant to current goals. Motivation, elicited by performance-contingent reward, reduces behavioural emotional distraction. In emotionally neutral contexts, reward is thought to encourage use of a proactive cognitive control strategy, altering anticipatory attentional settings to more effectively suppress distractors. The current preregistered study investigates whether a similar proactive shift occurs even when distractors are highly arousing emotional images. We monitored pupil area, an online measure of both cognitive and emotional processing, to examine how reward influences the time course of control. Participants (n = 110) identified a target letter flanking an irrelevant central image. Images were meaningless scrambles on 75% of trials; on the remaining 25%, they were intact positive (erotic), negative (mutilation), or neutral images. Half the participants received financial rewards for fast and accurate performance, while the other half received no performance-contingent reward. Emotional distraction was greater than neutral distraction, and both were attenuated by reward. Consistent with behavioural findings, pupil dilation was greater following emotional than neutral distractors, and dilation to intact distractors (regardless of valence) was decreased by reward. Although reward did not enhance tonic pupil dilation (an index of sustained proactive control), exploratory analyses showed that reward altered the time course of control—eliciting a sharp, rapid, increase in dilation immediately preceding stimulus onset (reflecting dynamic use of anticipatory control), that extended until well after stimulus offset. These findings suggest that reward alters the time course of control by encouraging proactive preparation to rapidly disengage from emotional distractors. |
Anita E. Wagner; Leanne Nagels; Paolo Toffanin; Jane M. Opie; Deniz Başkent Individual variations in effort: Assessing pupillometry for the hearing impaired Journal Article In: Trends in Hearing, vol. 23, 2019. @article{Wagner2019, Assessing effort in speech comprehension for hearing-impaired (HI) listeners is important, as effortful processing of speech can limit their hearing rehabilitation. We examined the measure of pupil dilation in its capacity to accommodate the heterogeneity that is present within clinical populations by studying lexical access in users with sensorineural hearing loss, who perceive speech via cochlear implants (CIs). We compared the pupillary responses of 15 experienced CI users and 14 age-matched normal-hearing (NH) controls during auditory lexical decision. A growth curve analysis was applied to compare the responses between the groups. NH listeners showed a coherent pattern of pupil dilation that reflects the task demands of the experimental manipulation and a homogenous time course of dilation. CI listeners showed more variability in the morphology of pupil dilation curves, potentially reflecting variable sources of effort across individuals. In follow-up analyses, we examined how speech perception, a task that relies on multiple stages of perceptual analyses, poses multiple sources of increased effort for HI listeners, wherefore we might not be measuring the same source of effort for HI as for NH listeners. We argue that interindividual variability among HI listeners can be clinically meaningful in attesting not only the magnitude but also the locus of increased effort. The understanding of individual variations in effort requires experimental paradigms that (a) differentiate the task demands during speech comprehension, (b) capture pupil dilation in its time course per individual listeners, and (c) investigate the range of individual variability present within clinical and NH populations. |
Rozemarijn S. Kleef; Claudi L. H. Bockting; Evelien Valen; André Aleman; Jan Bernard C. Marsman; Marie José Tol In: BMC Psychiatry, vol. 19, pp. 1–11, 2019. @article{Kleef2019, Background: Major Depressive Disorder (MDD) is a psychiatric disorder with a highly recurrent character, making prevention of relapse an important clinical goal. Preventive Cognitive Therapy (PCT) has been proven effective in preventing relapse, though not for every patient. A better understanding of relapse vulnerability and working mechanisms of preventive treatment may inform effective personalized intervention strategies. Neurocognitive models of MDD suggest that abnormalities in prefrontal control over limbic emotion-processing areas during emotional processing and regulation are important in understanding relapse vulnerability. Whether changes in these neurocognitive abnormalities are induced by PCT and thus play an important role in mediating the risk for recurrent depression, is currently unclear. In the Neurocognitive Working Mechanisms of the Prevention of Relapse In Depression (NEWPRIDE) study, we aim to 1) study neurocognitive factors underpinning the vulnerability for relapse, 2) understand the neurocognitive working mechanisms of PCT, 3) predict longitudinal treatment effects based on pre-treatment neurocognitive characteristics, and 4) validate the pupil dilation response as a marker for prefrontal activity, reflecting emotion regulation capacity and therapy success. Methods: In this randomized controlled trial, 75 remitted recurrent MDD (rrMDD) patients will be included. Detailed clinical and cognitive measurements, fMRI scanning and pupillometry will be performed at baseline and three-month follow-up. In the interval, 50 rrMDD patients will be randomized to eight sessions of PCT and 25 rrMDD patients to a waiting list. At baseline, 25 healthy control participants will be additionally included to objectify cross-sectional residual neurocognitive abnormalities in rrMDD. After 18 months, clinical assessments of relapse status are performed to investigate which therapy induced changes predict relapse in the 50 patients allocated to PCT. Discussion: The present trial is the first to study the neurocognitive vulnerability factors underlying relapse and mediating relapse prevention, their value for predicting PCT success and whether pupil dilation acts as a valuable marker in this regard. Ultimately, a deeper understanding of relapse prevention could contribute to the development of better targeted preventive interventions. Trial registration: Trial registration: Netherlands Trial Register, August 18, 2015, trial number NL5219. |
Laura Leuchs; Max Schneider; Victor I. Spoormaker Measuring the conditioned response: A comparison of pupillometry, skin conductance, and startle electromyography Journal Article In: Psychophysiology, vol. 56, no. 1, pp. e13283, 2019. @article{Leuchs2019, In human fear conditioning studies, different physiological readouts can be used to track conditioned responding during fear learning. Commonly employed readouts such as skin conductance responses (SCR) or startle responses have in recent years been complemented by pupillary readouts, but to date it is unknown how pupillary readouts relate to other measures of the conditioned response. To examine differences and communalities among pupil responses, SCR, and startle responses, we simultaneously recorded pupil diameter, skin conductance, and startle electromyography in 47 healthy subjects during fear acquisition, extinction, and a recall test on 2 consecutive days. The different measures correlated only weakly, displaying most prominent differences in their response patterns during fear acquisition. Whereas SCR and startle responses habituated, pupillary measures did not. Instead, they increased in response to fear conditioned stimuli and most closely followed ratings of unconditioned stimulus (US) expectancy. Moreover, we observed that startle-induced pupil responses showed stimulus discrimination during fear acquisition, suggesting a fear potentiation of the auditory pupil reflex. We conclude that different physiological outcome measures of the conditioned response inform about different cognitive-affective processes during fear learning, with pupil responses being least affected by physiological habituation and most closely following US expectancy. |
Robert Jagiello; Ulrich Pomper; Makoto Yoneya; Sijia Zhao; Maria Chait Rapid brain sesponses to familiar vs. unfamiliar music-an EEG and pupillometry study Journal Article In: Scientific Reports, vol. 9, pp. 15570, 2019. @article{Jagiello2019, Human listeners exhibit marked sensitivity to familiar music, perhaps most readily revealed by popular "name that tune" games, in which listeners often succeed in recognizing a familiar song based on extremely brief presentation. In this work, we used electroencephalography (EEG) and pupillometry to reveal the temporal signatures of the brain processes that allow differentiation between a familiar, well liked, and unfamiliar piece of music. In contrast to previous work, which has quantified gradual changes in pupil diameter (the so-called "pupil dilation response"), here we focus on the occurrence of pupil dilation events. This approach is substantially more sensitive in the temporal domain and allowed us to tap early activity with the putative salience network. Participants (N = 10) passively listened to snippets (750 ms) of a familiar, personally relevant and, an acoustically matched, unfamiliar song, presented in random order. A group of control participants (N = 12), who were unfamiliar with all of the songs, was also tested. We reveal a rapid differentiation between snippets from familiar and unfamiliar songs: Pupil responses showed greater dilation rate to familiar music from 100-300 ms post-stimulus-onset, consistent with a faster activation of the autonomic salience network. Brain responses measured with EEG showed a later differentiation between familiar and unfamiliar music from 350 ms post onset. Remarkably, the cluster pattern identified in the EEG response is very similar to that commonly found in the classic old/new memory retrieval paradigms, suggesting that the recognition of brief, randomly presented, music snippets, draws on similar processes. |
Katja Herrmann; Andreas Sprenger; Leoni Baumung; Daniel Alvarez-Fischer; Alexander Münchau; Valerie Brandt Help or hurt? How attention modulates tics under different conditions Journal Article In: Cortex, vol. 120, pp. 471–482, 2019. @article{Herrmann2019, Tourette syndrome is a neuropsychiatric developmental disorder, characterized by tics that are often preceded by an increasingly uncomfortable urge to move. Tic frequency can increase when patients pay attention to their tics, if tics are not suppressed. This study investigates how attentions modulates urge intensity, tic frequency and arousal during free ticcing and tic suppression. Tic frequency (video recording), urge intensity (rating scale) and pupil width (pupillometry as a measure of arousal) were assessed in 23 patients with Tourette syndrome (mean age 33.48 ± 12.37; 14 male) during five attention conditions: 1) baseline, 2) watching own tics in a live video-feedback, 3) watching own tics in a previously recorded video, 4) thinking about situations that can trigger tics and 5) thinking about specific, non-tic related stimuli (distraction condition) during: a) free ticcing and b) tic suppression tic states. Urge intensity and tic frequency increased in the free ticcing condition when patients viewed their own tics live and when they thought about tic-triggering situations. In the tic suppression condition, tic frequency increased when patients watched a video of their tics, thought about their tics or were distracted. Pupil width increased significantly during the live feedback and the video condition compared to baseline in both tic states. Paying attention to own tics can be detrimental when tics are not suppressed. In contrast, paying attention to other stimuli appears detrimental when tics are suppressed, as would be the case during most current behavioural therapy techniques. However, results point to high emotional arousal and patients feeling uncomfortable when seeing themselves tic. The results also suggest that urge intensity is modulated by changes in attention in the same manner as tics and may drive change in tic frequency during free ticcing. |
Dorothea Hämmerer; Philipp Schwartenbeck; Maria Gallagher; Thomas Henry Benedict FitzGerald; Emrah Düzel; Raymond Joseph Dolan Older adults fail to form stable task representations during model-based reversal inference Journal Article In: Neurobiology of Aging, vol. 74, pp. 90–100, 2019. @article{Haemmerer2019, Older adults struggle in dealing with changeable and uncertain environments across several cognitive domains. This has been attributed to difficulties in forming adequate task representations that help navigate uncertain environments. Here, we investigate how, in older adults, inadequate task representations impact on model-based reversal learning. We combined computational modeling and pupillometry during a novel model-based reversal learning task, which allowed us to isolate the relevance of task representations at feedback evaluation. We find that older adults overestimate the changeability of task states and consequently are less able to converge on unequivocal task representations through learning. Pupillometric measures and behavioral data show that these unreliable task representations in older adults manifest as a reduced ability to focus on feedback that is relevant for updating task representations, and as a reduced metacognitive awareness in the accuracy of their actions. Instead, the data suggested older adults' choice behavior was more consistent with a guidance by uninformative feedback properties such as outcome valence. Our study highlights that an inability to form adequate task representations may be a crucial factor underlying older adults' impaired model-based inference. |
Steven M. Gillespie; Pia Rotshtein; Harriet Chapman; Emmie Brown; Anthony R. Beech; Ian J. Mitchell Pupil reactivity to emotional faces among convicted violent offenders: The role of psychopathic traits Journal Article In: Journal of Abnormal Psychology, vol. 128, no. 6, pp. 622–632, 2019. @article{Gillespie2019, Psychopathy is characteristically associated with impairments in recognizing others' facial expressions of emotion, and there is some evidence that these difficulties are specific to the callousness features of the disorder. However, it remains unclear whether these difficulties are accompanied by reductions in autonomic reactivity when viewing others' emotional expressions, and whether these impairments are particular to expressions showing another's distress or are more pervasive across different emotional expressions. In this study, 73 adult male prisoners with histories of serious sexual or violent offenses- who ranged across the psychopathy continuum-completed a facial emotion recognition task. For the first time in a convicted offender sample, we used pupillometry techniques to measure changes in the pupil dilation response, a measure of sympathetic autonomic arousal to affective stimuli. We found that the callousness features of psychopathy were related to impaired recognition of fearful faces. Strikingly, we also showed that increasing callousness was associated with a reduction in the pupil dilation response and that this was pervasive across different emotional expressions. Our results highlight a potential role of the locus coeruleus-noradrenaline system in the pathophysiology of psychopathy and demonstrate the potential of the pupillary response as a technique for understanding attention- emotion interactions in psychopathy. |
Abraham I. J. Gajardo; Samuel Madariaga; Pedro E. Maldonado Autonomic nervous system assessment by pupillary response as a potential biomarker for cardiovascular risk: A pilot study Journal Article In: Journal of Clinical Neuroscience, vol. 59, pp. 41–46, 2019. @article{Gajardo2019, Background: Cardiovascular risk (CVR) biomarkers are of increasing interest because of their potential utility in management of cardiovascular diseases. The activity of the autonomic nervous system (ANS) is known to be highly correlated with CVR and therefore, is a putative biomarker. Common ANS measurement tools have several technological limitations and high-variance signals. The pupillary responses (PR) is controlled by both components of the ANS, and recent advances in pupillometry are making this measurement, easy and reliable. Thus, PR assessment could become a useful clinical tool to measure the ANS modulation and its relation to CVR. Here, we aimed to evaluate differences in PR between low CVR and moderate/high CVR individuals. Methods: We performed a cross-sectional study. We recruited voluntaries with low CVR (group 1 |
Daniel L. Bowling; Pablo Graf Ancochea; Michael J. Hove; W. Tecumseh Fitch Pupillometry of groove: Evidence for noradrenergic arousal in the link between music and movement Journal Article In: Frontiers in Neuroscience, vol. 12, pp. 1039, 2019. @article{Bowling2019, The capacity to entrain motor action to rhythmic auditory stimulation is highly developed in humans and extremely limited in our closest relatives. Investigating the mechanisms underlying this capacity thus represents an opportunity to advance our understanding of human evolution. An important aspect of auditory-motor entrainment is that not all forms of rhythmic stimulation motivate movement to the same degree. This variation is captured by the concept of musical groove: high-groove music stimulates a strong desire for movement, whereas low-groove music does not. Here, we utilize this difference to investigate the neurophysiological basis of our capacity for auditory-motor entrainment. In a series of three experiments we examine pupillary responses to musical stimuli varying in groove. Our results show stronger pupil dilation in response to (1) high- vs. low-groove music, (2) high vs. low spectral content, and (3) syncopated vs. straight drum patterns. We additionally report evidence for consistent sex differences in music-induced pupillary responses, with males exhibiting larger differences between responses, but females exhibiting stronger responses overall. These results imply that the biological link between movement and auditory rhythms in our species is supported by the capacity of high-groove music to stimulate arousal in the central and peripheral nervous system, presumably via highly conserved noradrenergic mechanisms. |
Sara Alhanbali; Piers Dawes; Rebecca E. Millman; Kevin J. Munro Measures of listening effort are multidimensional Journal Article In: Ear & Hearing, vol. 40, no. 5, pp. 1084–1097, 2019. @article{Alhanbali2019, OBJECTIVES: Listening effort can be defined as the cognitive resources required to perform a listening task. The literature on listening effort is as confusing as it is voluminous: measures of listening effort rarely correlate with each other and sometimes result in contradictory findings. Here, we directly compared simultaneously recorded multimodal measures of listening effort. After establishing the reliability of the measures, we investigated validity by quantifying correlations between measures and then grouping-related measures through factor analysis. DESIGN: One hundred and sixteen participants with audiometric thresholds ranging from normal to severe hearing loss took part in the study (age range: 55 to 85 years old, 50.3% male). We simultaneously measured pupil size, electroencephalographic alpha power, skin conductance, and self-report listening effort. One self-report measure of fatigue was also included. The signal to noise ratio (SNR) was adjusted at 71% criterion performance using sequences of 3 digits. The main listening task involved correct recall of a random digit from a sequence of six presented at a SNR where performance was around 82 to 93%. Test-retest reliability of the measures was established by retesting 30 participants 7 days after the initial session. RESULTS: With the exception of skin conductance and the self-report measure of fatigue, interclass correlation coefficients (ICC) revealed good test-retest reliability (minimum ICC: 0.71). Weak or nonsignificant correlations were identified between measures. Factor analysis, using only the reliable measures, revealed four underlying dimensions: factor 1 included SNR, hearing level, baseline alpha power, and performance accuracy; factor 2 included pupillometry; factor 3 included alpha power (during speech presentation and during retention); factor 4 included self-reported listening effort and baseline alpha power. CONCLUSIONS: The good ICC suggests that poor test reliability is not the reason for the lack of correlation between measures. We have demonstrated that measures traditionally used as indicators of listening effort tap into multiple underlying dimensions. We therefore propose that there is no "gold standard" measure of listening effort and that different measures of listening effort should not be used interchangeably. When choosing method(s) to measure listening effort, the nature of the task and aspects of increased listening demands that are of interest should be taken into account. The findings of this study provide a framework for understanding and interpreting listening effort measures. |
2018 |
Matthew B. Winn; Ashley N. Moore In: Trends in Hearing, vol. 22, 2018. @article{Winn2018, Contextual cues can be used to improve speech recognition, especially for people with hearing impairment. However, previous work has suggested that when the auditory signal is degraded, context might be used more slowly than when the signal is clear. This potentially puts the hearing-impaired listener in a dilemma of continuing to process the last sentence when the next sentence has already begun. This study measured the time course of the benefit of context using pupillary responses to high- and low-context sentences that were followed by silence or various auditory distractors (babble noise, ignored digits, or attended digits). Participants were listeners with cochlear implants or normal hearing using a 12-channel noise vocoder. Context-related differences in pupil dilation were greater for normal hearing than for cochlear implant listeners, even when scaled for differences in pupil reactivity. The benefit of context was systematically reduced for both groups by the presence of the later-occurring sounds, including virtually complete negation when sentences were followed by another attended utterance. These results challenge how we interpret the benefit of context in experiments that present just one utterance at a time. If a listener uses context to ‘‘repair'' part of a sentence, and later-occurring auditory stimuli interfere with that repair process, the benefit of context might not survive outside the idealized laboratory or clinical environment. Elevated listening effort in hearing-impaired listeners might therefore result not just from poor auditory encoding but also inefficient use of context and prolonged processing of misperceived utterances competing with perception of incoming speech. |
Jorrig Vogels; Vera Demberg; Jutta Kray The index of cognitive activity as a measure of cognitive processing load in dual task settings Journal Article In: Frontiers in Psychology, vol. 9, pp. 2276, 2018. @article{Vogels2018, Increases in pupil size have long been used as an indicator of cognitive load. Recently, the Index of Cognitive Activity (ICA), a novel pupillometric measure has received increased attention. The ICA measures the frequency of rapid pupil dilations, and is an interesting complementary measure to overall pupil size because it disentangles the pupil response to cognitive activity from effects of light input. As such, it has been evaluated as a useful measure of processing load in dual task settings coordinating language comprehension and driving. However, the cognitive underpinnings of pupillometry, and any differences between rapid small dilations as measured by the ICA and overall effects on pupil size are still poorly understood. Earlier work has observed that the ICA and overall pupil size may not always behave in the same way, reporting an increase in overall pupil size but decrease in ICA in a dual task setting. To further investigate this, we systematically tested two new dual-task combinations, combining both language comprehension and simulated driving with a memory task. Our findings confirm that more difficult linguistic processing is reflected in a larger ICA. More importantly, however, the dual task settings did not result in an increase in the ICA as compared to the single task, and, consistent with earlier findings, showed a significant decrease with a more difficult secondary task. This contrasts with our findings for pupil size, which showed an increase with greater secondary task difficulty in both tasks. Our results are compatible with the idea that although both pupillometry measures are indicators of cognitive load, they reflect different cognitive and neuronal processes in dual task situations. |
Joanne C. Van Slooten; Sara Jahfari; Tomas Knapen; Jan Theeuwes How pupil responses track value-based decision-making during and after reinforcement learning Journal Article In: PLoS Computational Biology, vol. 14, no. 11, pp. e1006632, 2018. @article{VanSlooten2018, Cognition can reveal itself in the pupil, as latent cognitive processes map onto specific pupil responses. For instance, the pupil dilates when we make decisions and these pupil size fluctuations reflect decision-making computations during and after a choice. Surprisingly little is known, however, about how pupil responses relate to decisions driven by the learned value of stimuli. This understanding is important, as most real-life decisions are guided by the outcomes of earlier choices. The goal of this study was to investigate which cognitive processes the pupil reflects during value-based decision-making. We used a reinforcement learning task to study pupil responses during value-based decisions and subsequent decision evaluations, employing computational modeling to quantitatively describe the underlying cognitive processes. We found that the pupil closely tracks reinforcement learning processes independently across participants and across trials. Prior to choice, the pupil dilated as a function of trial-by-trial fluctuations in value beliefs about the to-be chosen option and predicted an individual's tendency to exploit high value options. After feedback a biphasic pupil response was observed, the amplitude of which correlated with participants' learning rates. Furthermore, across trials, early feedback-related dilation scaled with value uncertainty, whereas later constriction scaled with signed reward prediction errors. These findings show that pupil size fluctuations can provide detailed information about the computations underlying value-based decisions and the subsequent updating of value beliefs. As these processes are affected in a host of psychiatric disorders, our results indicate that pupillometry can be used as an accessible tool to non-invasively study the processes underlying ongoing reinforcement learning in the clinic. |
Marco Turi; David C. Burr; Paola Binda Pupillometry reveals perceptual differences that are tightly linked to autistic traits in typical adults Journal Article In: eLife, vol. 7, pp. 1–15, 2018. @article{Turi2018, The pupil is primarily regulated by prevailing light levels but is also modulated by perceptual and attentional factors. We measured pupil-size in typical adult humans viewing a bistable-rotating cylinder, constructed so the luminance of the front surface changes with perceived direction of rotation. In some participants, pupil diameter oscillated in phase with the ambiguous perception, more dilated when the black surface was in front. Importantly, the magnitude of oscillation predicts autistic traits of participants, assessed by the Autism-Spectrum Quotient AQ. Further experiments suggest that these results are driven by differences in perceptual styles: high AQ participants focus on the front surface of the rotating cylinder, while those with low AQ distribute attention to both surfaces in a more global, holistic style. This is the first evidence that pupillometry reliably tracks inter-individual differences in perceptual styles; it does so quickly and objectively, without interfering with spontaneous perceptual strategies. |
Max Schneider; Laura Leuchs; Michael Czisch; Philipp G. Sämann; Victor I. Spoormaker Disentangling reward anticipation with simultaneous pupillometry / fMRI Journal Article In: NeuroImage, vol. 178, pp. 11–22, 2018. @article{Schneider2018, The reward system may provide an interesting intermediate phenotype for anhedonia in affective disorders. Reward anticipation is characterized by an increase in arousal, and previous studies have linked the anterior cingulate cortex (ACC) to arousal responses such as dilation of the pupil. Here, we examined pupil dynamics during a reward anticipation task in forty-six healthy human subjects and evaluated its neural correlates using functional magnetic resonance imaging (fMRI). Pupil size showed a strong increase during monetary reward anticipation, a moderate increase during verbal reward anticipation and a decrease during control trials. For fMRI analyses, average pupil size and pupil change were computed in 1-s time bins during the anticipation phase. Activity in the ventral striatum was inversely related to the pupil size time course, indicating an early onset of activation and a role in reward prediction processing. Pupil dilations were linked to increased activity in the salience network (dorsal ACC and bilateral insula), which likely triggers an increase in arousal to enhance task performance. Finally, increased pupil size preceding the required motor response was associated with activity in the ventral attention network. In sum, pupillometry provides an effective tool for disentangling different phases of reward anticipation, with relevance for affective symptomatology. |
Anne Reuten; Maureen Dam; Marnix Naber Pupillary responses to robotic and human emotions: The uncanny valley and media equation confirmed Journal Article In: Frontiers in Psychology, vol. 9, pp. 774, 2018. @article{Reuten2018, Physiological responses during human-robots interaction are useful alternatives to subjective measures of uncanny feelings for nearly humanlike robots (uncanny valley) and comparable emotional responses between humans and robots (media equation). However, no studies have employed the easily accessible measure of pupillometry to confirm the uncanny valley and media equation hypotheses, evidence in favor of the existence of these hypotheses in interaction with emotional robots is scarce, and previous studies have not controlled for low level image statistics across robot appearances. We therefore recorded pupil size of 40 participants that viewed and rated pictures of robotic and human faces that expressed a variety of basic emotions. The robotic faces varied along the dimension of human likeness from cartoonish to humanlike. We strictly controlled for confounding factors by removing backgrounds, hair, and color, and by equalizing low level image statistics. After the presentation phase, participants indicated to what extent the robots appeared uncanny and humanlike, and whether they could imagine social interaction with the robots in real life situations. The results show that robots rated as nearly humanlike scored higher on uncanniness, scored lower on imagined social interaction, evoked weaker pupil dilations, and their emotional expressions were more difficult to recognize. Pupils dilated most strongly to negative expressions and the pattern of pupil responses across emotions was highly similar between robot and human stimuli. These results highlight the usefulness of pupillometry in emotion studies and robot design by confirming the uncanny valley and media equation hypotheses. |
Eliska Prochazkova; Luisa Prochazkova; Michael Rojek Giffin; H. Steven Scholte; Carsten K. W. De Dreu; Mariska E. Kret Pupil mimicry promotes trust through the theory-of-mind network Journal Article In: Proceedings of the National Academy of Sciences, vol. 115, no. 31, pp. E7265–E7274, 2018. @article{Prochazkova2018, The human eye can provide powerful insights into the emotions and intentions of others; however, how pupillary changes influence observers' behavior remains largely unknown. The present fMRI–pupillometry study revealed that when the pupils of interacting partners synchronously dilate, trust is promoted, which suggests that pupil mimicry affiliates people. Here we provide evidence that pupil mimicry modulates trust decisions through the activation of the theory-of-mind network (precuneus, temporo-parietal junction, superior temporal sulcus, and medial prefrontal cortex). This network was recruited during pupil-dilation mimicry compared with interactions without mimicry or compared with pupil-constriction mimicry. Furthermore, the level of theory-of-mind engagement was proportional to individual's susceptibility to pupil-dilation mimicry. These data reveal a fundamental mechanism by which an individual's pupils trigger neurophysiological responses within an observer: when interacting partners synchronously dilate their pupils, humans come to feel reflections of the inner states of others, which fosters trust formation. |
Daniel R. McCloy; Eric D. Larson; Adrian K. C. Lee Auditory attention switching with listening difficulty: Behavioral and pupillometric measures Journal Article In: The Journal of the Acoustical Society of America, vol. 144, no. 5, pp. 2764–2771, 2018. @article{McCloy2018, Pupillometry has emerged as a useful tool for studying listening effort. Past work involving listeners with normal audiological thresholds has shown that switching attention between competing talker streams evokes pupil dilation indicative of listening effort [McCloy, Lau, Larson, Pratt, and Lee (2017). J. Acoust. Soc. Am. 141(4), 2440–2451]. The current experiment examines behavioral and pupillometric data from a two-stream target detection task requiring attention-switching between auditory streams, in two participant groups: audiometrically normal listeners who self-report difficulty localizing sound sources and/or understanding speech in reverberant or acoustically crowded environments, and their age-matched controls who do not report such problems. Three experimental conditions varied the number and type of stream segregation cues available. Participants who reported listening difficulty showed both behavioral and pupillometric signs of increased effort compared to controls, especially in trials where only a single stream segregation cue was available |
Sebastiaan Mathôt; Jasper H. Fabius; Elle Van Heusden; Stefan Van der Stigchel Safe and sensible preprocessing and baseline correction of pupil-size data Journal Article In: Behavior Research Methods, vol. 50, no. 1, pp. 94–106, 2018. @article{Mathot2018, Measurement of pupil size (pupillometry) has recently gained renewed interest from psychologists, but there is little agreement on how pupil-size data is best analyzed. Here we focus on one aspect of pupillometric analyses: baseline correction, i.e., analyzing changes in pupil size relative to a baseline period. Baseline correction is useful in experiments that investigate the effect of some experimental manipulation on pupil size. In such experiments, baseline correction improves statistical power by taking into account random fluctuations in pupil size over time. However, we show that baseline correction can also distort data if unrealistically small pupil sizes are recorded during the baseline period, which can easily occur due to eye blinks, data loss, or other distortions. Divisive baseline correction (corrected pupil size = pupil size/baseline) is affected more strongly by such distortions than subtractive baseline correction (corrected pupil size = pupil size - baseline). We discuss the role of baseline correction as a part of preprocessing of pupillometric data, and make five recommendations: (1) before baseline correction, perform data preprocessing to mark missing and invalid data, but assume that some distortions will remain in the data; (2) use subtractive baseline correction; (3) visually compare your corrected and uncorrected data; (4) be wary of pupil-size effects that emerge faster than the latency of the pupillary response allows (within ±220 ms after the manipulation that induces the effect); and (5) remove trials on which baseline pupil size is unrealistically small (indicative of blinks and other distortions). |
Katja I. Häuser; Vera Demberg; Jutta Kray In: Psychology and Aging, vol. 33, no. 8, pp. 1168–1180, 2018. @article{Haeuser2018, Even though older adults are known to have difficulty at language processing when a secondary task has to be performed simultaneously, few studies have addressed how older adults process language in dual-task demands when linguistic load is systematically varied. Here, we manipulated surprisal, an information theoretic measure that quantifies the amount of new information conveyed by a word, to investigate how linguistic load affects younger and older adults during early and late stages of sentence processing under conditions when attention is split between two tasks. In high-surprisal sentences, target words were implausible and mismatched with semantic expectancies based on context, thereby causing integration difficulty. Participants performed semantic meaningfulness judgments on sentences that were presented in isolation (single task) or while performing a secondary tracking task (dual task). Cognitive load was measured by means of pupillometry. Mixed-effects models were fit to the data, showing the following: (a) During the dual task, younger but not older adults demonstrated early sensitivity to surprisal (higher levels of cognitive load, indexed by pupil size) as sentences were heard online; (b) Older adults showed no immediate reaction to surprisal, but a delayed response, where their meaningfulness judgments to high-surprisal words remained stable in accuracy, while secondary tracking performance declined. Findings are discussed in relation to age-related trade-offs in dual tasking and differences in the allocation of attentional resources during language processing. Collectively, our data show that higher linguistic load leads to task trade-offs in older adults and differently affects the time course of online language processing in aging. |
Lauren K. Fink; Brian K. Hurley; Joy J. Geng; Petr Janata A linear oscillator model predicts dynamic temporal attention and pupillary entrainment to rhythmic patterns Journal Article In: Journal of Eye Movement Research, vol. 11, no. 2, pp. 1–25, 2018. @article{Fink2018, Rhythm is a ubiquitous feature of music that induces specific neural modes of processing. In this paper, we assess the potential of a stimulus-driven linear oscillator model (Tomic & Janata, 2008) to predict dynamic attention to complex musical rhythms on an instant-by-instant basis. We use perceptual thresholds and pupillometry as attentional indices against which to test our model predictions. During a deviance detection task, participants listened to continuously looping, multi-instrument, rhythmic patterns, while being eye-tracked. Their task was to respond anytime they heard an increase in intensity (dB SPL). An adaptive thresholding algorithm adjusted deviant intensity at multiple probed temporal locations throughout each rhythmic stimulus. The oscillator model predicted participants' perceptual thresholds for detecting deviants at probed locations, with a low temporal salience prediction corresponding to a high perceptual threshold and vice versa. A pupil dilation response was observed for all deviants. Notably, the pupil dilated even when partic- ipants did not report hearing a deviant. Maximum pupil size and resonator model output were significant predictors of whether a deviant was detected or missed on any given trial. Besides the evoked pupillary response to deviants, we also assessed the continuous pupillary signal to the rhythmic patterns. The pupil exhibited entrainment at prominent periodicities present in the stimuli and followed each of the different rhythmic patterns in a unique way. Overall, these results replicate previous studies using the linear oscillator model to predict dynamic attention to complex auditory scenes and extend the utility of the model to the prediction of neurophysiological signals, in this case the pupillary time course; however, we note that the amplitude envelope of the acoustic patterns may serve as a similarly useful predictor. To our knowledge, this is the first paper to show entrainment of pupil dynamics by demonstrating a phase relationship between musical stimuli and the pupillary signal. |
Garvin Brod; Marcus Hasselhorn; Silvia A. Bunge When generating a prediction boosts learning: The element of surprise Journal Article In: Learning and Instruction, vol. 55, pp. 22–31, 2018. @article{Brod2018, Using both behavioral and eye-tracking methodology, we tested whether and how asking students to generate predictions is an efficient technique to improve learning. In particular, we designed two tasks to test whether the surprise induced by outcomes that violate expectations enhances learning. Data from the first task revealed that asking participants to generate predictions, as compared to making post hoc evaluations, facilitated acquisition of geography knowledge. Pupillometry measurements revealed that expectancy-violating outcomes led to a surprise response only when a prediction was made beforehand, and that the strength of this response was positively related to the amount of learning. Data from the second task demonstrated that making predictions about the outcomes of soccer matches specifically improved memory for expectancy-violating events. These results suggest that a specific benefit of making predictions in learning contexts is that it creates the opportunity for the learner to be surprised. Implications for theory and educational practice are discussed. |
Giulia Borghini; Valerie Hazan Listening effort during sentence processing is increased for non-native listeners: A pupillometry study Journal Article In: Frontiers in Neuroscience, vol. 12, pp. 152, 2018. @article{Borghini2018, Current evidence demonstrates that even though some non-native listeners can achieve native-like performance for speech perception tasks in quiet, the presence of a background noise is much more detrimental to speech intelligibility for non-native compared to native listeners. Even when performance is equated across groups, it is likely that greater listening effort is required for non-native listeners. Importantly, the added listening effort might result in increased fatigue and a reduced ability to successfully perform multiple tasks simultaneously. Task-evoked pupil responses have been demonstrated to be a reliable measure of cognitive effort and can be useful in clarifying those aspects. In this study we compared the pupil response for 23 native English speakers and 27 Italian speakers of English as a second language. Speech intelligibility was tested for sentences presented in quiet and in background noise at two performance levels that were matched across groups. Signal-to-noise levels corresponding to these sentence intelligibility levels were pre-determined using an adaptive intelligibility task. Pupil response was significantly greater in non-native compared to native participants across both intelligibility levels. Therefore, for a given intelligibility level, a greater listening effort is required when listening in a second language in order to understand speech in noise. Results also confirmed that pupil response is sensitive to speech intelligibility during language comprehension, in line with previous research. However, contrary to our predictions, pupil response was not differentially modulated by intelligibility levels for native and non-native listeners. The present study corroborates that pupillometry can be deemed as a valid measure to be used in speech perception investigation, because it is sensitive to differences both across participants, such as listener type, and across conditions, such as variations in the level of speech intelligibility. Importantly, pupillometry offers us the possibility to uncover differences in listening effort even when those do not emerge in the performance level of individuals. |
Vladislav Ayzenberg; Meghan R. Hickey; Stella F. Lourenco Pupillometry reveals the physiological underpinnings of the aversion to holes Journal Article In: PeerJ, vol. 6, pp. 1–19, 2018. @article{Ayzenberg2018, An unusual, but common, aversion to images with clusters of holes is known as trypophobia. Recent research suggests that trypophobic reactions are caused by visual spectral properties also present in aversive images of evolutionary threatening animals (e.g., snakes and spiders). However, despite similar spectral properties, it remains unknown whether there is a shared emotional response to holes and threatening animals. Whereas snakes and spiders are known to elicit a fear reaction, associated with the sympathetic nervous system, anecdotal reports from self-described trypophobes suggest reactions more consistent with disgust, which is associated with activation of the parasympathetic nervous system. Here we used pupillometry in a novel attempt to uncover the distinct emotional response associated with a trypophobic response to holes. Across two experiments, images of holes elicited greater constriction compared to images of threatening animals and neutral images. Moreover, this effect held when controlling for level of arousal and accounting for the pupil grating response. This pattern of pupillary response is consistent with involvement of the parasympathetic nervous system and suggests a disgust, not a fear, response to images of holes. Although general aversion may be rooted in shared visual-spectral properties, we propose that the specific emotion is determined by cognitive appraisal of the distinct image content. |
Nicolai D. Ayasse; Arthur Wingfield A tipping point in listening effort: Effects of linguistic complexity and age-related hearing loss on sentence comprehension Journal Article In: Trends in Hearing, vol. 22, 2018. @article{Ayasse2018, In recent years, there has been a growing interest in the relationship between effort and performance. Early formulations implied that, as the challenge of a task increases, individuals will exert more effort, with resultant maintenance of stable performance. We report an experiment in which normal-hearing young adults, normal-hearing older adults, and older adults with age-related mild-to-moderate hearing loss were tested for comprehension of recorded sentences that varied the comprehension challenge in two ways. First, sentences were constructed that expressed their meaning either with a simpler subject-relative syntactic structure or a more computationally demanding object-relative structure. Second, for each sentence type, an adjectival phrase was inserted that created either a short or long gap in the sentence between the agent performing an action and the action being performed. The measurement of pupil dilation as an index of processing effort showed effort to increase with task difficulty until a difficulty tipping point was reached. Beyond this point, the measurement of pupil size revealed a commitment of effort by the two groups of older adults who failed to keep pace with task demands as evidenced by reduced comprehension accuracy. We take these pupillometry data as revealing a complex relationship between task difficulty, effort, and performance that might not otherwise appear from task performance alone. |
2017 |
Mahiko Konishi; Kevin Brown; Luca Battaglini; Jonathan Smallwood When attention wanders: Pupillometric signatures of fluctuations in external attention Journal Article In: Cognition, vol. 168, pp. 16–26, 2017. @article{Konishi2017, Attention is not always directed to events in the external environment. On occasion our thoughts wander to people and places distant from the here and now. Sometimes, this lack of external attention can compromise ongoing task performance. In the current study we set out to understand the extent to which states of internal and external attention can be determined using pupillometry as an index of ongoing cognition. In two experiments we found that periods of slow responding were associated with elevations in the baseline pupil signal over three and a half seconds prior to a behavioural response. In the second experiment we found that unlike behavioural lapses, states of off-task thought, particularly those associated with a focus on the past and with an intrusive quality, were associated with reductions in the size of the pupil over the same window prior to the probe. These data show that both states of large and small baseline pupil size are linked to states when attention is not effectively focused on the external environment, although these states have different qualities. More generally, these findings illustrate that subjective and objective markers of task performance may not be equivalent and underscore the importance of developing objective indicators that can allow these different states to be understood. |
Alejandra Vasquez-Rosati; Enzo P. Brunetti; Carmen Cordero; Pedro E. Maldonado Pupillary response to negative emotional stimuli is differentially affected in meditation practitioners Journal Article In: Frontiers in Human Neuroscience, vol. 11, pp. 209, 2017. @article{VasquezRosati2017, Clinically, meditative practices have become increasingly relevant, decreasing anxiety in patients and increasing antibody production. However, few studies have examined the physiological correlates, or effects of the incorporation of meditative practices. Because pupillary reactivity is a marker for autonomic changes and emotional processing, we hypothesized that the pupillary responses of mindfulness meditation practitioners (MP) and subjects without such practices (NM differ, reflecting different emotional processing. In a group of 11 MP and 9 NM, we recorded the pupil diameter using video-oculography while subjects explored images with emotional contents. Although both groups showed a similar pupillary response for positive and neutral images, negative images evoked a greater pupillary contraction and a weaker dilation in the MP group. Also, this group had faster physiological recovery to baseline levels. These results suggest that mindfulness meditation practices modulate the response of the autonomic nervous system, reflected in the pupillary response to negative images and faster physiological recovery to baseline levels, suggesting that pupillometry could be used to assess the potential health benefits of these practices in patients. |
Martina Starc; Alan Anticevic; Grega Repovš Fine-grained versus categorical: Pupil size differentiates between strategies for spatial working memory performance Journal Article In: Psychophysiology, vol. 54, no. 5, pp. 724–735, 2017. @article{Starc2017, Pupillometry provides an accessible option to track working memory processes with high temporal resolution. Several studies showed that pupil size increases with the number of items held in working memory; however, no study has explored whether pupil size also reflects the quality of working memory representations. To address this question, we used a spatial working memory task to investigate the relationship of pupil size with spatial precision of responses and indicators of reliance on generalized spatial categories. We asked 30 participants (15 female, aged 19–31) to remember the position of targets presented at various locations along a hidden radial grid. After a delay, participants indicated the remembered location with a high-precision joystick providing a parametric measure of trial-to-trial accuracy. We recorded participants' pupil dilations continuously during task performance. Results showed a significant relation between pupil dilation during preparation/early encoding and the precision of responses, possibly reflecting the attentional resources devoted to memory encoding. In contrast, pupil dilation at late maintenance and response predicted larger shifts of responses toward prototypical locations, possibly reflecting larger reliance on categorical representation. On an intraindividual level, smaller pupil dilations during encoding predicted larger dilations during late maintenance and response. On an interindividual level, participants relying more on categorical representation also produced larger precision errors. The results confirm the link between pupil size and the quality of spatial working memory representation. They suggest compensatory strategies of spatial working memory performance—loss of precise spatial representation likely increases reliance on generalized spatial categories. |
Ronan McGarrigle; Piers Dawes; Andrew J. Stewart; Stefanie E. Kuchinsky; Kevin J. Munro Pupillometry reveals changes in physiological arousal during a sustained listening task Journal Article In: Psychophysiology, vol. 54, no. 2, pp. 193–203, 2017. @article{McGarrigle2017a, Hearing loss is associated with anecdotal reports of fatigue during periods of sustained listening. However, few studies have attempted to measure changes in arousal, as a potential marker of fatigue, over the course of a sustained listening task. The present study aimed to examine subjective, behavioral, and physiological indices of listening-related fatigue. Twenty-four normal-hearing young adults performed a speech-picture verification task in different signal-to-noise ratios (SNRs) while their pupil size was monitored and response times recorded. Growth curve analysis revealed a significantly steeper linear decrease in pupil size in the more challenging SNR, but only in the second half of the trial block. Changes in pupil dynamics over the course of the more challenging listening condition block suggest a reduction in physiological arousal. Behavioral and self-report measures did not reveal any differences between listening conditions. This is the first study to show reduced physiological arousal during a sustained listening task, with changes over time consistent with the onset of fatigue. |
Ronan McGarrigle; Piers Dawes; Andrew J. Stewart; Stefanie E. Kuchinsky; Kevin J. Munro Measuring listening-related effort and fatigue in school-aged children using pupillometry Journal Article In: Journal of Experimental Child Psychology, vol. 161, pp. 95–112, 2017. @article{McGarrigle2017, Stress and fatigue from effortful listening may compromise well-being, learning, and academic achievement in school-aged children. The aim of this study was to investigate the effect of a signal-to-noise ratio (SNR) typical of those in school classrooms on listening effort (behavioral and pupillometric) and listening-related fatigue (self-report and pupillometric) in a group of school-aged children. A sample of 41 normal-hearing children aged 8–11 years performed a narrative speech–picture verification task in a condition with recommended levels of background noise (“ideal”: +15 dB SNR) and a condition with typical classroom background noise levels (“typical”: −2 dB SNR). Participants showed increased task-evoked pupil dilation in the typical listening condition compared with the ideal listening condition, consistent with an increase in listening effort. No differences were found between listening conditions in terms of performance accuracy and response time on the behavioral task. Similarly, no differences were found between listening conditions in self-report and pupillometric markers of listening-related fatigue. This is the first study to (a) examine listening-related fatigue in children using pupillometry and (b) demonstrate physiological evidence consistent with increased listening effort while listening to spoken narratives despite ceiling-level task performance accuracy. Understanding the physiological mechanisms that underpin listening-related effort and fatigue could inform intervention strategies and ultimately mitigate listening difficulties in children. |
Daniel R. McCloy; Bonnie K. Lau; Eric D. Larson; Katherine A. I. Pratt; Adrian K. C. Lee Pupillometry shows the effort of auditory attention switching Journal Article In: The Journal of the Acoustical Society of America, vol. 141, no. 4, pp. 2440–2451, 2017. @article{McCloy2017, © 2017 Acoustical Society of America. Successful speech communication often requires selective attention to a target stream amidst competing sounds, as well as the ability to switch attention among multiple interlocutors. However, auditory attention switching negatively affects both target detection accuracy and reaction time, suggesting that attention switches carry a cognitive cost. Pupillometry is one method of assessing mental effort or cognitive load. Two experiments were conducted to determine whether the effort associated with attention switches is detectable in the pupillary response. In both experiments, pupil dilation, target detection sensitivity, and reaction time were measured; the task required listeners to either maintain or switch attention between two concurrent speech streams. Secondary manipulations explored whether switch-related effort would increase when auditory streaming was harder. In experiment 1, spatially distinct stimuli were degraded by simulating reverberation (compromising across-time streaming cues), and target-masker talker gender match was also varied. In experiment 2, diotic streams separable by talker voice quality and pitch were degraded by noise vocoding, and the time alloted for mid-trial attention switching was varied. All trial manipulations had some effect on target detection sensitivity and/or reaction time; however, only the attention-switching manipulation affected the pupillary response: greater dilation was observed in trials requiring switching attention between talkers. |
Laura Leuchs; Max Schneider; Michael Czisch; Victor I. Spoormaker Neural correlates of pupil dilation during human fear learning Journal Article In: NeuroImage, vol. 147, pp. 186–197, 2017. @article{Leuchs2017, Background: Fear conditioning and extinction are prevailing experimental and etiological models for normal and pathological anxiety. Pupil dilations in response to conditioned stimuli are increasingly used as a robust psychophysiological readout of fear learning, but their neural correlates remain unknown. We aimed at identifying the neural correlates of pupil responses to threat and safety cues during a fear learning task. Methods: Thirty-four healthy subjects underwent a fear conditioning and extinction paradigm with simultaneous functional magnetic resonance imaging (fMRI) and pupillometry. After a stringent preprocessing and artifact rejection procedure, trial-wise pupil responses to threat and safety cues were entered as parametric modulations to the fMRI general linear models. Results: Trial-wise magnitude of pupil responses to both conditioned and safety stimuli correlated positively with activity in dorsal anterior cingulate cortex (dACC), thalamus, supramarginal gyrus and insula for the entire fear learning task, and with activity in the dACC during the fear conditioning phase in particular. Phasic pupil responses did not show habituation, but were negatively correlated with tonic baseline pupil diameter, which decreased during the task. Correcting phasic pupil responses for the tonic baseline pupil diameter revealed thalamic activity, which was also observed in an analysis employing a linear (declining) time modulation. Conclusion: Pupil dilations during fear conditioning and extinction provide useful readouts to track fear learning on a trial-by-trial level, particularly with simultaneous fMRI. Whereas phasic pupil responses reflect activity in brain regions involved in fear learning and threat appraisal, most prominently in dACC, tonic changes in pupil diameter may reflect changes in general arousal. |
Piril Hepsomali; Julie A. Hadwin; Simon P. Liversedge; Matthew Garner Pupillometric and saccadic measures of affective and executive processing in anxiety Journal Article In: Biological Psychology, vol. 127, pp. 173–179, 2017. @article{Hepsomali2017, Anxious individuals report hyper-arousal and sensitivity to environmental stimuli, difficulties concentrating, performing tasks efficiently and inhibiting unwanted thoughts and distraction. We used pupillometry and eye-movement measures to compare high vs. low anxious individuals hyper-reactivity to emotional stimuli (facial expressions) and subsequent attentional biases in a memory-guided pro- and antisaccade task during conditions of low and high cognitive load (short vs. long delay). High anxious individuals produced larger and slower pupillary responses to face stimuli, and more erroneous eye-movements, particularly following long delay. Low anxious individuals' pupillary responses were sensitive to task demand (reduced during short delay), whereas high anxious individuals' were not. These findings provide evidence in anxiety of enhanced, sustained and inflexible patterns of pupil responding during affective stimulus processing and cognitive load that precede deficits in task performance. |
Juan Haro; Marc Guasch; Blanca Vallès; Pilar Ferré Is pupillary response a reliable index of word recognition? Evidence from a delayed lexical decision task Journal Article In: Behavior Research Methods, vol. 49, no. 5, pp. 1930–1938, 2017. @article{Haro2017, Previous word recognition studies have shown that the pupillary response is sensitive to a word's frequency. However, such a pupillary effect may be due to the process of executing a response, instead of being an index of word processing. With the aim of exploring this possibility, we recorded the pupillary responses in two experiments involving a lexical decision task (LDT). In the first experiment, participants completed a standard LDT, whereas in the second they performed a delayed LDT. The delay in the response allowed us to compare pupil dilations with and without the response execution component. The results showed that pupillary response was modulated by word frequency in both the standard and the delayed LDT. This finding supports the reliability of using pupillometry for word recognition research. Importantly, our results also suggest that tasks that do not require a response during pupil recording lead to clearer and stronger effects. |
Marc Guasch; Pilar Ferré; Juan Haro Pupil dilation is sensitive to the cognate status of words: Further evidence for non-selectivity in bilingual lexical access Journal Article In: Bilingualism: Language and Cognition, vol. 20, no. 1, pp. 49–54, 2017. @article{Guasch2017, The cognate facilitation effect (i.e., a processing advantage for cognates compared to non-cognates) is an evidence of language non-selectivity in bilingual lexical access. Several studies using behavioral or electrophysiological measures have demonstrated that this effect is modulated by the degree of formal overlap between translations. However, it has never been tested with a psychophysiological measure such as pupillometry. In the present study we replicate the cognate facilitation effect by examining reaction times and pupil responses. Our results endorse pupillometry as a promising tool for bilingual research, and confirm the modulation of the cognate effect by the degree of formal similarity. |
Eugen Fischer; Paul E. Engelhardt Stereotypical inferences: Philosophical relevance and psycholinguistic toolkit Journal Article In: Ratio, vol. 30, no. 4, pp. 411–442, 2017. @article{Fischer2017, Stereotypes shape inferences in philosophical thought, political discourse, and everyday life. These inferences are routinely made when thinkers engage in language comprehension or production: We make them whenever we hear, read, or formulate stories, reports, philosophical case-descriptions, or premises of arguments – on virtually any topic. These inferences are largely automatic: largely unconscious, non-intentional, and effortless. Accordingly, they shape our thought in ways we can properly understand only by complementing traditional forms of philosophical analysis with experimental methods from psycholinguistics. This paper seeks, first, to bring out the wider philosophical relevance of stereotypical inference, well beyond familiar topics like gender and race. Second, we wish to provide (experimental) philosophers with a toolkit to experimentally study these ubiquitous inferences and what intuitions they may generate. This paper explains what stereotypes are (Section 1), and why they matter to current and traditional concerns in philosophy – experimental, analytic, and applied (Section 2). It then assembles a psycholinguistic toolkit and demonstrates through two studies (Sections 3–4) how potentially questionnairebased measures (plausibility-ratings) can be combined with process measures (reaction times and pupillometry) to garner evidence for specific stereotypical inferences and study when they ‘go through' and influence our thinking. |
Nathaniel T. Diede; Julie M. Bugg Cognitive effort is modulated outside of the explicit awareness of conflict frequency: Evidence from pupillometry Journal Article In: Journal of Experimental Psychology: Learning, Memory, and Cognition, vol. 43, no. 5, pp. 824–835, 2017. @article{Diede2017, Classic theories of cognitive control conceptualized controlled processes as slow, strategic, and willful, with automatic processes being fast and effortless. The context-specific proportion compatibility (CSPC) effect, the reduction in the compatibility effect in a context (e.g., location) associated with a high relative to low likelihood of conflict, challenged classic theories by demonstrating fast and flexible control that appears to operate outside of conscious awareness. Two theoretical questions yet to be addressed are whether the CSPC effect is accompanied by context-dependent variation in effort, and whether the exertion of effort depends on explicit awareness of context-specific task demands. To address these questions, pupil diameter was measured during a CSPC paradigm. Stimuli were randomly presented in either a mostly compatible location or a mostly incompatible location. Replicating prior research, the CSPC effect was found. The novel finding was that pupil diameter was greater in the mostly incompatible location compared to the mostly compatible location, despite participants' lack of awareness of context-specific task demands. Additionally, this difference occurred regardless of trial type or a preceding switch in location. These patterns support the view that context (location) dictates selection of optimal attentional settings in the CSPC paradigm, and varying levels of effort and performance accompany these settings. Theoretically, these patterns imply that cognitive control may operate fast, flexibly, and outside of awareness, but not effortlessly. |
Árni Gunnar Ásgeirsson; Sander Nieuwenhuis No arousal-biased competition in focused visuospatial attention Journal Article In: Cognition, vol. 168, pp. 191–204, 2017. @article{Asgeirsson2017, Arousal sometimes enhances and sometimes impairs perception and memory. A recent theory attempts to reconcile these findings by proposing that arousal amplifies the competition between stimulus representations, strengthening already strong representations and weakening already weak representations. Here, we report a stringent test of this arousal-biased competition theory in the context of focused visuospatial attention. Participants were required to identify a briefly presented target in the context of multiple distractors, which varied in the degree to which they competed for representation with the target, as revealed by psychophysics. We manipulated arousal using emotionally arousing pictures (Experiment 1), alerting tones (Experiment 2) and white-noise stimulation (Experiment 3), and validated these manipulations with electroencephalography and pupillometry. In none of the experiments did we find evidence that arousal modulated the effect of distractor competition on the accuracy of target identification. Bayesian statistics revealed moderate to strong evidence against arousal-biased competition. Modeling of the psychophysical data based on Bundesen's (1990) theory of visual attention corroborated the conclusion that arousal does not bias competition in focused visuospatial attention. |
Kelly Miles; Catherine M. McMahon; Isabelle Boisvert; Ronny Ibrahim; Peter Lissa; Petra L. Graham; Björn Lyxell Objective assessment of listening effort: Coregistration of pupillometry and EEG Journal Article In: Trends in Hearing, vol. 21, 2017. @article{Miles2017, Listening to speech in noise is effortful, particularly for people with hearing impairment. While it is known that effort is related to a complex interplay between bottom-up and top-down processes, the cognitive and neurophysiological mechan-isms contributing to effortful listening remain unknown. Therefore, a reliable physiological measure to assess effort remains elusive. This study aimed to determine whether pupil dilation and alpha power change, two physiological measures suggested to index listening effort, assess similar processes. Listening effort was manipulated by parametrically varying spectral reso-lution (16-and 6-channel noise vocoding) and speech reception thresholds (SRT; 50% and 80%) while 19 young, normal-hearing adults performed a speech recognition task in noise. Results of off-line sentence scoring showed discrepancies between the target SRTs and the true performance obtained during the speech recognition task. For example, in the SRT80% condition, participants scored an average of 64.7%. Participants' true performance levels were therefore used for subsequent statistical modelling. Results showed that both measures appeared to be sensitive to changes in spectral reso-lution (channel vocoding), while pupil dilation only was also significantly related to their true performance levels (%) and task accuracy (i.e., whether the response was correctly or partially recalled). The two measures were not correlated, suggesting they each may reflect different cognitive processes involved in listening effort. This combination of findings contributes to a growing body of research aiming to develop an objective measure of listening effort. |
2016 |
Michael W. Weiss; Sandra E. Trehub; E. Glenn Schellenberg; Peter Habashi Pupils dilate for vocal or familiar music Journal Article In: Journal of Experimental Psychology: Human Perception and Performance, vol. 42, no. 8, pp. 1061–1065, 2016. @article{Weiss2016, Previous research reveals that vocal melodies are remembered better than instrumental renditions. Here we explored the possibility that the voice, as a highly salient stimulus, elicits greater arousal than nonvocal stimuli, resulting in greater pupil dilation for vocal than for instrumental melodies. We also explored the possibility that pupil dilation indexes memory for melodies. We tracked pupil dilation during a single exposure to 24 unfamiliar folk melodies (half sung to la la, half piano) and during a subsequent recognition test in which the previously heard melodies were intermixed with 24 novel melodies (half sung, half piano) from the same corpus. Pupil dilation was greater for vocal melodies than for piano melodies in the exposure phase and in the test phase. It was also greater for previously heard melodies than for novel melodies. Our findings provide the first evidence that pupillometry can be used to measure recognition of stimuli that unfold over several seconds. They also provide the first evidence of enhanced arousal to vocal melodies during encoding and retrieval, thereby supporting the more general notion of the voice as a privileged signal. |
Basil Wahn; Daniel P. Ferris; W. David Hairston; Peter König Pupil sizes scale with attentional load and task experience in a multiple object tracking task Journal Article In: PLoS ONE, vol. 11, no. 12, pp. e0168087, 2016. @article{Wahn2016a, Previous studies have related changes in attentional load to pupil size modulations. How-ever, studies relating changes in attentional load and task experience on a finer scale to pupil size modulations are scarce. Here, we investigated how these changes affect pupil sizes. To manipulate attentional load, participants covertly tracked between zero and five objects among several randomly moving objects on a computer screen. To investigate effects of task experience, the experiment was conducted on three consecutive days. We found that pupil sizes increased with each increment in attentional load. Across days, we found systematic pupil size reductions. We compared the model fit for predicting pupil size modulations using attentional load, task experience, and task performance as predictors. We found that a model which included attentional load and task experience as predictors had the best model fit while adding performance as a predictor to this model reduced the overall model fit. Overall, results suggest that pupillometry provides a viable metric for pre-cisely assessing attentional load and task experience in visuospatial tasks. |
Anita E. Wagner; Paolo Toffanin; Deniz Baskent The timing and effort of lexical access in natural and degraded speech Journal Article In: Frontiers in Psychology, vol. 7, pp. 398, 2016. @article{Wagner2016, Understanding speech is effortless in ideal situations, and although adverse conditions, such as caused by hearing impairment, often render it an effortful task, they do not necessarily suspend speech comprehension. A prime example of this is speech perception by cochlear implant users, whose hearing prostheses transmit speech as a significantly degraded signal. It is yet unknown how mechanisms of speech processing deal with such degraded signals, and whether they are affected by effortful processing of speech. This paper compares the automatic process of lexical competition between natural and degraded speech, and combines gaze fixations, which capture the course of lexical disambiguation, with pupillometry, which quantifies the mental effort involved in processing speech. Listeners' ocular responses were recorded during disambiguation of lexical embeddings with matching and mismatching durational cues. Durational cues were selected due to their substantial role in listeners' quick limitation of the number of lexical candidates for lexical access in natural speech. Results showed that lexical competition increased mental effort in processing natural stimuli in particular in presence of mismatching cues. Signal degradation reduced listeners' ability to quickly integrate durational cues in lexical selection, and delayed and prolonged lexical competition. The effort of processing degraded speech was increased overall, and because it had its sources at the pre-lexical level this effect can be attributed to listening to degraded speech rather than to lexical disambiguation. In sum, the course of lexical competition was largely comparable for natural and degraded speech, but showed crucial shifts in timing, and different sources of increased mental effort. We argue that well-timed progress of information from sensory to pre-lexical and lexical stages of processing, which is the result of perceptual adaptation during speech development, is the reason why in ideal situations speech is perceived as an undemanding task. Degradation of the signal or the receiver channel can quickly bring this well-adjusted timing out of balance and lead to increase in mental effort. Incomplete and effortful processing at the early pre-lexical stages has its consequences on lexical processing as it adds uncertainty to the forming and revising of lexical hypotheses. |
Johanne Tromp; Peter Hagoort; Antje S. Meyer Pupillometry reveals increased pupil size during indirect request comprehension Journal Article In: Quarterly Journal of Experimental Psychology, vol. 69, no. 6, pp. 1093–1108, 2016. @article{Tromp2016, Fluctuations in pupil size have been shown to reflect variations in processing demands during lexical and syntactic processing in language comprehension. An issue that has not received attention is whether pupil size also varies due to pragmatic manipulations. In two pupillometry experiments, we investigated whether pupil diameter was sensitive to increased processing demands as a result of comprehending an indirect request versus a direct statement. Adult participants were presented with 120 picture-sentence combinations that could be interpreted either as an indirect request (a picture of a window with the sentence "it's very hot here") or as a statement (a picture of a window with the sentence "it's very nice here"). Based on the hypothesis that understanding indirect utterances requires additional inferences to be made on the part of the listener, we predicted a larger pupil diameter for indirect requests than statements. The results of both experiments are consistent with this expectation. We suggest that the increase in pupil size reflects additional processing demands for the comprehension of indirect requests as compared to statements. This research demonstrates the usefulness of pupillometry as a tool for experimental research in pragmatics. |
Max Schneider; Pamela Hathway; Laura Leuchs; Philipp G. Sämann; Michael Czisch; Victor I. Spoormaker Spontaneous pupil dilations during the resting state are associated with activation of the salience network Journal Article In: NeuroImage, vol. 139, pp. 189–201, 2016. @article{Schneider2016, Resting state functional magnetic resonance imaging (rs-fMRI) is increasingly applied for the development of functional biomarkers in brain disorders. Recent studies have revealed spontaneous vigilance drifts during the resting state, involving changes in brain activity and connectivity that challenge the validity of uncontrolled rs-fMRI findings. In a combined rs-fMRI/eye tracking study, the pupil size of 32 healthy subjects after 2 h of sleep restriction was recorded as an indirect index for activity of the locus coeruleus, the brainstem's noradrenergic arousal center. The spontaneous occurrence of pupil dilations, but not pupil size per se, was associated with increased activity of the salience network, thalamus and frontoparietal regions. In turn, spontaneous constrictions of the pupil were associated with increased activity in visual and sensorimotor regions. These results were largely replicated in a sample of 36 healthy subjects who did not undergo sleep restriction, although in this sample the correlation between thalamus and pupil dilation fell below whole-brain significance. Our data show that spontaneous pupil fluctuations during rest are indeed associated with brain circuitry involved in tonic alertness and vigilance. Pupillometry is an effective method to control for changes in tonic alertness during rs-fMRI. |
Sameer Saproo; Victor Shih; David C. Jangraw; Paul Sajda Neural mechanisms underlying catastrophic failure in human-machine interaction during aerial navigation Journal Article In: Journal of Neural Engineering, vol. 13, pp. 1–12, 2016. @article{Saproo2016, Objective. We investigated the neural correlates of workload buildup in a fine visuomotor task called the boundary avoidance task (BAT). The BAT has been known to induce naturally occurring failures of human–machine coupling in high performance aircraft that can potentially lead to a crash—these failures are termed pilot induced oscillations (PIOs). Approach. We recorded EEG and pupillometry data from human subjects engaged in a flight BAT simulated within a virtual 3D environment. Main results. We find that workload buildup in a BAT can be successfully decoded from oscillatory features in the electroencephalogram (EEG). Information in delta, theta, alpha, beta, and gamma spectral bands of the EEG all contribute to successful decoding, however gamma band activity with a lateralized somatosensory topography has the highest contribution, while theta band activity with a fronto-central topography has the most robust contribution in terms of real-world usability. We show that the output of the spectral decoder can be used to predict PIO susceptibility. We also find that workload buildup in the task induces pupil dilation, the magnitude of which is significantly correlated with the magnitude of the decoded EEG signals. These results suggest that PIOs may result from the dysregulation of cortical networks such as the locus coeruleus (LC)—anterior cingulate cortex (ACC) circuit. Significance. Our findings may generalize to similar control failures in other cases of tight manmachine coupling where gains and latencies in the control system must be inferred and compensated for by the human operators. A closed-loop intervention using neurophysiological decoding of workload buildup that targets the LC-ACC circuit may positively impact operator performance in such situations. |
Sebastiaan Mathôt; Jean-Baptiste Melmi; Lotje Linden; Stefan Van Der Stigchel The mind-writing pupil: A human-computer interface based on decoding of covert attention through pupillometry Journal Article In: PLoS ONE, vol. 11, no. 2, pp. e0148805, 2016. @article{Mathot2016, We present a new human-computer interface that is based on decoding of attention through pupillometry. Our method builds on the recent finding that covert visual attention affects the pupillary light response: Your pupil constricts when you covertly (without looking at it) attend to a bright, compared to a dark, stimulus. In our method, participants covertly attend to one of several letters with oscillating brightness. Pupil size reflects the brightness of the selected letter, which allows us–with high accuracy and in real time–to determine which letter the par- ticipant intends to select. The performance of our method is comparable to the best covert- attention brain-computer interfaces to date, and has several advantages: no movement other than pupil-size change is required; no physical contact is required (i.e. no electrodes); it is easy to use; and it is reliable. Potential applications include: communication with totally locked-in patients, training of sustained attention, and ultra-secure password input. |
Gary J. Lewis; Timothy C. Bates In: Journal of Cognitive Neuroscience, vol. 28, no. 2, pp. 308–318, 2016. @article{Lewis2016, The ability to adaptively shift between exploration and exploitation control states is critical for optimizing behavioral performance. Converging evidence from primate electrophysiology and computational neural modeling has suggested that this ability may be mediated by the broad norepinephrine projections emanating from the locus coeruleus (LC) [Aston-Jones, G., & Cohen, J. D. An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28, 403–450, 2005]. There is also evidence that pupil diameter covaries systematically with LC activity. Although imperfect and indirect, this link makes pupillometry a useful tool for studying the locus coeruleus norepinephrine system in humans and in high-level tasks. Here, we present a novel paradigm that examines how the pupillary response during exploration and exploitation covaries with individual differences in fluid intelligence during analogical reasoning on Raven's Advanced Progressive Matrices. Pupillometry was used as a noninvasive proxy for LC activity, and concurrent think-aloud verbal protocols were used to identify exploratory and exploitative solution periods. This novel combination of pupillometry and verbal protocols from 40 participants revealed a decrease inpupil diameter during exploitation and an increase during exploration. The temporal dynamics of the pupillary response was characterized by a steep increase during the transition to exploratory periods, sustained dilation for many seconds afterward, and followed by gradual return to baseline.Moreover, the individual differences in the relative magnitude of pupillary dilation accounted for 16% of the variance in Advanced Progressive Matrices scores. Assuming that pupil diameter is a valid index of LC activity, these results establish promising preliminary connections between the literature on locus coeruleus norepinephrine-mediated cognitive control and the literature on analogical reasoning and fluid intelligence. |
Markos Kyritsis; Stephen R. Gulliver; Eva Feredoes Environmental factors and features that influence visual search in a 3D WIMP interface Journal Article In: International Journal of Human-Computer Studies, vol. 92-93, pp. 30–43, 2016. @article{Kyritsis2016, The challenge of moving past the classic Window Icons Menus Pointer (WIMP) interface, i.e. by turning it '3D', has resulted in much research and development. To evaluate the impact of 3D on the 'finding a target picture in a folder' task, we built a 3D WIMP interface that allowed the systematic manipulation of visual depth, visual aides, semantic category distribution of targets versus non-targets; and the detailed measurement of lower-level stimuli features. Across two separate experiments, one large sample web-based experiment, to understand associations, and one controlled lab environment, using eye tracking to understand user focus, we investigated how visual depth, use of visual aides, use of semantic categories, and lower-level stimuli features (i.e. contrast, colour and luminance) impact how successfully participants are able to search for, and detect, the target image. Moreover in the lab-based experiment, we captured pupillometry measurements to allow consideration of the influence of increasing cognitive load as a result of either an increasing number of items on the screen, or due to the inclusion of visual depth. Our findings showed that increasing the visible layers of depth, and inclusion of converging lines, did not impact target detection times, errors, or failure rates. Low-level features, including colour, luminance, and number of edges, did correlate with differences in target detection times, errors, and failure rates. Our results also revealed that semantic sorting algorithms significantly decreased target detection times. Increased semantic contrasts between a target and its neighbours correlated with an increase in detection errors. Finally, pupillometric data did not provide evidence of any correlation between the number of visible layers of depth and pupil size, however, using structural equation modelling, we demonstrated that cognitive load does influence detection failure rates when there is luminance contrasts between the target and its surrounding neighbours. Results suggest that WIMP interaction designers should consider stimulus-driven factors, which were shown to influence the efficiency with which a target icon can be found in a 3D WIMP interface. |
Phillip D. Fletcher; Jennifer M. Nicholas; Laura E. Downey; Hannah L. Golden; Camilla N. Clark; Carolina Pires; Jennifer L. Agustus; Catherine J. Mummery; Jonathan M. Schott; Jonathan D. Rohrer; Sebastian J. Crutch; Jason D. Warren A physiological signature of sound meaning in dementia Journal Article In: Cortex, vol. 77, pp. 13–23, 2016. @article{Fletcher2016, The meaning of sensory objects is often behaviourally and biologically salient and decoding of semantic salience is potentially vulnerable in dementia. However, it remains unclear how sensory semantic processing is linked to physiological mechanisms for coding object salience and how that linkage is affected by neurodegenerative diseases. Here we addressed this issue using the paradigm of complex sounds. We used pupillometry to compare physiological responses to real versus synthetic nonverbal sounds in patients with canonical dementia syndromes (behavioural variant frontotemporal dementia - bvFTD, semantic dementia - SD; progressive nonfluent aphasia - PNFA; typical Alzheimer's disease - AD) relative to healthy older individuals. Nonverbal auditory semantic competence was assessed using a novel within-modality sound classification task and neuroanatomical associations of pupillary responses were assessed using voxel-based morphometry (VBM) of patients' brain MR images. After taking affective stimulus factors into account, patients with SD and AD showed significantly increased pupil responses to real versus synthetic sounds relative to healthy controls. The bvFTD, SD and AD groups had a nonverbal auditory semantic deficit relative to healthy controls and nonverbal auditory semantic performance was inversely correlated with the magnitude of the enhanced pupil response to real versus synthetic sounds across the patient cohort. A region of interest analysis demonstrated neuroanatomical associations of overall pupil reactivity and differential pupil reactivity to sound semantic content in superior colliculus and left anterior temporal cortex respectively. Our findings suggest that autonomic coding of auditory semantic ambiguity in the setting of a damaged semantic system may constitute a novel physiological signature of neurodegenerative diseases. |
Federica Bianchi; Sébastien Santurette; Dorothea Wendt; Torsten Dau Pitch discrimination in musicians and non-musicians: Effects of harmonic resolvability and processing effort Journal Article In: JARO - Journal of the Association for Research in Otolaryngology, vol. 17, no. 1, pp. 69–79, 2016. @article{Bianchi2016, Musicians typically show enhanced pitch discrimination abilities compared to non-musicians. The present study investigated this perceptual enhancement behaviorally and objectively for resolved and unresolved complex tones to clarify whether the enhanced performance in musicians can be ascribed to increased peripheral frequency selectivity and/or to a different processing effort in performing the task. In a first experiment, pitch discrimination thresholds were obtained for harmonic complex tones with fundamental frequencies (F0s) between 100 and 500 Hz, filtered in either a low- or a high-frequency region, leading to variations in the resolvability of audible harmonics. The results showed that pitch discrimination performance in musicians was enhanced for resolved and unresolved complexes to a similar extent. Additionally, the harmonics became resolved at a similar F0 in musicians and non-musicians, suggesting similar peripheral frequency selectivity in the two groups of listeners. In a follow-up experiment, listeners' pupil dilations were measured as an indicator of the required effort in performing the same pitch discrimination task for conditions of varying resolvability and task difficulty. Pupillometry responses indicated a lower processing effort in the musicians versus the non-musicians, although the processing demand imposed by the pitch discrimination task was individually adjusted according to the behavioral thresholds. Overall, these findings indicate that the enhanced pitch discrimination abilities in musicians are unlikely to be related to higher peripheral frequency selectivity and may suggest an enhanced pitch representation at more central stages of the auditory system in musically trained listeners. |
2015 |
Eefje W. M. Rondeel; Henk Steenbergen; Rob W. Holland; Ad Knippenberg A closer look at cognitive control: differences in resource allocation during updating, inhibition and switching as revealed by pupillometry Journal Article In: Frontiers in Human Neuroscience, vol. 9, pp. 494, 2015. @article{Rondeel2015, The present study investigated resource allocation, as measured by pupil dilation, in tasks measuring updating (2-Back task), inhibition (Stroop task) and switching (Number Switch task). Because each cognitive control component has unique characteristics, differences in patterns of resource allocation were expected. Pupil and behavioral data from 35 participants were analyzed. In the 2-Back task (requiring correct matching of current stimulus identity at trial p with the stimulus two trials back, p -2) we found that better performance (low total of errors made in the task) was positively correlated to the mean pupil dilation during correctly responding to targets. In the Stroop task, pupil dilation on incongruent trials was higher than those on congruent trials. Incongruent vs. congruent trial pupil dilation differences were positively related to reaction time differences between incongruent and congruent trials. Furthermore, on congruent Stroop trials, pupil dilation was negatively related to reaction times, presumably because more effort allocation paid off in terms of faster responses. In addition, pupil dilation on correctly-responded-to congruent trials predicted a weaker Stroop interference effect in terms of errors, probably because pupil dilation on congruent trials were diagnostic of task motivation, resulting in better performance. In the Number Switch task we found higher pupil dilation in switch as compared to non-switch trials. On the Number Switch task, pupil dilation was not related to performance. We also explored error-related pupil dilation in all tasks. The results provide new insights in the diversity of the cognitive control components in terms of resource allocation as a function of individual differences, task difficulty and error processing. |
Frieder M. Paulus; Sören Krach; Marius Blanke; Christine Roth; Marcus Belke; Jens Sommer; Laura Müller-Pinzler; Katja Menzler; Andreas Jansen; Felix Rosenow; Frank Bremmer; Wolfgang Einhäuser; Susanne Knake Fronto-insula network activity explains emotional dysfunctions in juvenile myoclonic epilepsy: Combined evidence from pupillometry and fMRI Journal Article In: Cortex, vol. 65, pp. 219–231, 2015. @article{Paulus2015, Emotional instability, difficulties in social adjustment, and disinhibited behavior are the most common symptoms of the psychiatric comorbidities in juvenile myoclonic epilepsy (JME). This psychopathology has been associated with dysfunctions of mesial-frontal brain circuits. The present work is a first direct test of this link and adapted a paradigm for probing frontal circuits during empathy for pain. Neural and psychophysiological parameters of pain empathy were assessed by combining functional magnetic resonance imaging (fMRI) with simultaneous pupillometry in 15 JME patients and 15 matched healthy controls. In JME patients, we observed reduced neural activation of the anterior cingulate cortex (ACC), the anterior insula (AI), and the ventrolateral prefrontal cortex (VLPFC). This modulation was paralleled by reduced pupil dilation during empathy for pain in patients. At the same time, pupil dilation was positively related to neural activity of the ACC, AI, and VLPFC. In JME patients, the ACC additionally showed reduced functional connectivity with the primary and secondary somatosensory cortex, areas fundamentally implicated in processing the somatic cause of another's pain. Our results provide first evidence that alterations of mesial-frontal circuits directly affect psychosocial functioning in JME patients and draw a link of pupil dynamics with brain activity during emotional processing. The findings of reduced pain empathy related activation of the ACC and AI and aberrant functional integration of the ACC with somatosensory cortex areas provide further evidence for this network's role in social behavior and helps explaining the JME psychopathology and patients' difficulties in social adjustment. |
Sebastiaan Mathôt; Jean-Baptiste Melmi; Eric Castet Intrasaccadic perception triggers pupillary constriction Journal Article In: PeerJ, vol. 3, pp. 1–16, 2015. @article{Mathot2015, It is commonly believed that vision is impaired during saccadic eye movements. However, here we report that some visual stimuli are clearly visible during saccades, and trigger a constriction of the eye's pupil. Participants viewed sinusoid gratings that changed polarity 150 times per second (every 6.67 ms). At this rate of flicker, the gratings were perceived as homogeneous surfaces while participants fixated. However, the flickering gratings contained ambiguous motion: rightward and leftward motion for vertical gratings; upward and downward motion for horizontal gratings. When participants made a saccade perpendicular to the gratings' orientation (e.g., a leftward saccade for a vertical grating), the eye's peak velocity matched the gratings' motion. As a result, the retinal image was approximately stable for a brief moment during the saccade, and this gave rise to an intrasaccadic percept: A normally invisible stimulus became visible when eye velocity was maximal. Our results confirm and extend previous studies by demonstrating intrasaccadic perception using a reflexive measure (pupillometry) that does not rely on subjective report. Our results further show that intrasaccadic perception affects all stages of visual processing, from the pupillary response to visual awareness. |
Sören Krach; Inge Kamp-Becker; Wolfgang Einhäuser; Jens Sommer; Stefan Frässle; Andreas Jansen; Lena Rademacher; Laura Müller-Pinzler; Valeria Gazzola; Frieder M. Paulus Evidence from pupillometry and fMRI indicates reduced neural response during vicarious social pain but not physical pain in autism Journal Article In: Human Brain Mapping, vol. 36, no. 11, pp. 4730–4744, 2015. @article{Krach2015, Autism spectrum disorder (ASD) is characterized by substantial social deficits. The notion that dysfunctions in neural circuits involved in sharing another's affect explain these deficits is appealing, but has received only modest experimental support. Here we evaluated a complex paradigm on the vicarious social pain of embarrassment to probe social deficits in ASD as to whether it is more potent than paradigms currently in use. To do so we acquired pupillometry and fMRI in young adults with ASD and matched healthy controls. During a simple vicarious physical pain task no differences emerged between groups in behavior, pupillometry, and neural activation of the anterior insula (AIC) and anterior cingulate cortex (ACC). In contrast, processing complex vicarious social pain yielded reduced responses in ASD on all physiological measures of sharing another's affect. The reduced activity within the AIC was thereby explained by the severity of autistic symptoms in the social and affective domain. Additionally, behavioral responses lacked correspondence with the anterior cingulate and anterior insula cortex activity found in controls. Instead, behavioral responses in ASD were associated with hippocampal activity. The observed dissociation echoes the clinical observations that deficits in ASD are most pronounced in complex social situations and simple tasks may not probe the dysfunctions in neural pathways involved in sharing affect. Our results are highly relevant because individuals with ASD may have preserved abilities to share another's physical pain but still have problems with the vicarious representation of more complex emotions that matter in life. |
Kai Kaspar; Vanessa Krapp; Peter König Hand washing induces a clean slate effect in moral judgments: A pupillometry and eye-tracking study Journal Article In: Scientific Reports, vol. 5, pp. 10471, 2015. @article{Kaspar2015a, Physical cleansing is commonly understood to protect us against physical contamination. However, recent studies showed additional effects on moral judgments. Under the heading of the "Macbeth effect" direct links between bodily cleansing and one's own moral purity have been demonstrated. Here we investigate (1) how moral judgments develop over time and how they are altered by hand washing, (2) whether changes in moral judgments can be explained by altered information sampling from the environment, and (3) whether hand washing affects emotional arousal. Using a pre-post control group design, we found that morality ratings of morally good and bad scenes acquired more extreme values in the control group over time, an effect that was fully counteracted by intermediate hand washing. This result supports the notion of a clean slate effect by hand washing. Thereby, eye-tracking data did not uncover differences in eye movement behavior that may explain differences in moral judgments. Thus, the clean slate effect is not due to altered information sampling from the environment. Finally, compared to the control group, pupil diameter decreased after hand washing, thus demonstrating a direct physiological effect. The results shed light on the physiological mechanisms behind this type of embodiment phenomenon. |