Adrian Andrzej Chrobak; Bartosz Bohaterewicz; Anna Maria Sobczak; Magdalena Marszał-Wiśniewska; Anna Tereszko; Anna Krupa; Anna Ceglarek; Magdalena Fafrowicz; Amira Bryll; Tadeusz Marek; Dominika Dudek; Marcin Siwek
Time-frequency characterization of resting brain in bipolar disorder during euthymia - A preliminary study Journal Article
In: Brain Sciences, vol. 11, no. 5, pp. 599, 2021.
The goal of this paper is to investigate the baseline brain activity in euthymic bipolar disorder (BD) patients by comparing it to healthy controls (HC) with the use of a variety of resting state functional magnetic resonance imaging (rs-fMRI) analyses, such as amplitude of low frequency fluctuations (ALFF), fractional ALFF (f/ALFF), ALFF-based functional connectivity (FC), and r egional homogeneity (ReHo). We hypothesize that above-mentioned techniques will differentiate BD from HC indicating dissimilarities between the groups within different brain structures. Forty-two participants divided into two groups of euthymic BD patients (n = 21) and HC (n = 21) underwent rs-fMRI evaluation. Typical band ALFF, slow-4, slow-5, f/ALFF, as well as ReHo indexes were analyzed. Regions with altered ALFF were chosen as ROI for seed-to-voxel analysis of FC. As opposed to HC, BD patients revealed: increased ALFF in left insula; increased slow-5 in left middle temporal pole; increased f/ALFF in left superior frontal gyrus, left superior temporal gyrus, left middle occipital gyrus, right putamen, and bilateral thalamus. There were no significant differences between BD and HC groups in slow-4 band. Compared to HC, the BD group presented higher ReHo values in the left superior medial frontal gyrus and lower ReHo values in the right supplementary motor area. FC analysis revealed significant hyper-connectivity within the BD group between left insula and bilateral middle frontal gyrus, right superior parietal gyrus, right supramarginal gyrus, left inferior parietal gyrus, left cerebellum, and left supplementary motor area. To our best knowledge, this is the first rs-fMRI study combining ReHo, ALFF, f/ALFF, and subdivided frequency bands (slow-4 and slow-5) in euthymic BD patients. ALFF, f/ALFF, slow-5, as well as REHO analysis revealed significant differences between two studied groups. Although results obtained with the above methods enable to identify group-specific brain structures, no overlap between the brain regions was detected. This indicates that combination of foregoing rs-fMRI methods may complement each other, revealing the bigger picture of the complex resting state abnormalities in BD.
Jongik Chung; Brooke S. Jackson; Jennifer E. Mcdowell; Cheolwoo Park
Joint estimation and regularized aggregation of brain network in FMRI data Journal Article
In: Journal of Neuroscience Methods, vol. 364, pp. 109374, 2021.
Background: In the Gaussian graphical model framework, precision matrices reveal conditional dependence structure among random variables. In functional magnetic resonance imaging (fMRI) data, estimating such precision matrices of multi-subjects and aggregating them to a group-level is an essential step for constructing a group brain network. New method: In this article, we considered joint estimation of multiple precision matrices with regularized aggregation. Also, in the construction of a group precision matrix, we integrated robust aggregation to the estimation. In the estimation of individual precision matrices, we took a regularization approach to induce sparsity, which made brain network estimation more realistic. Results: We demonstrated the effectiveness of the proposed method through simulated examples, and analyses on real fMRI data acquired during eye movement tasks assessing cognitive control. For the fMRI data, the joint estimation of multiple precision matrices (JEMP) with regularized aggregation (RA) captured more robust associations between task-relevant neural regions of interest (ROIs), compared to the analyses using JEMP alone. The JEMP with RA also was sensitive to increased neural efficiency after task practice. Comparison with existing method(s): The simple average of individual precision matrices may be affected by outliers and provide inconsistent outcomes between subject-level and group-level networks. In contrast, the proposed method yielded a robust group graph that could identify and ease the effect of outliers. Conclusions: The proposed method identified regions of practice-induced attenuation associated with reduced cognitive demand after repeat task exposure. Through simulated and real data, we demonstrated that this method does not require any distribution assumption, can identify outliers, and provides robust, representative group brain networks. This method can be applied to datasets that have extensive variability and/or multiple outliers, including applications to specific, and general, cognitive processes, as well as for studies that may require longitudinal data, such as pharmaceutical trials.
Benjamin Haas; Martin I. Sereno; D. Samuel Schwarzkopf
Inferior occipital gyrus is organized along common gradients of spatial and face-part selectivity Journal Article
In: Journal of Neuroscience, vol. 41, no. 25, pp. 5511–5521, 2021.
The ventral visual stream of the human brain is subdivided into patches with categorical stimulus preferences, like faces or scenes. However, the functional organization within these areas is less clear. Here, we used functional magnetic resonance imaging and vertex-wise tuning models to independently probe spatial and face-part preferences in the inferior occipital gyrus (IOG) of healthy adult males and females. The majority of responses were well explained by Gaussian population tuning curves for both retinotopic location and the preferred relative position within a face. Parameter maps revealed a common gradient of spatial and face-part selectivity, with the width of tuning curves drastically increasing from posterior to anterior IOG. Tuning peaks clustered more idiosyncratically but were also correlated across maps of visual and face space. Preferences for the upper visual field went along with significantly increased coverage of the upper half of the face, matching recently discovered biases in human perception. Our findings reveal a broad range of neural face-part selectivity in IOG, ranging from narrow to “holistic.” IOG is functionally organized along this gradient, which in turn is correlated with retinotopy.
J. A. Elshout; D. P. Bergsma; A. V. Berg; K. V. Haak
Functional MRI of visual cortex predicts training-induced recovery in stroke patients with homonymous visual field defects Journal Article
In: NeuroImage: Clinical, vol. 31, pp. 102703, 2021.
Post-chiasmatic damage to the visual system leads to homonymous visual field defects (HVDs), which can severely interfere with daily life activities. Visual Restitution Training (VRT) can recover parts of the affected visual field in patients with chronic HVDs, but training outcome is variable. An untested hypothesis suggests that training potential may be largest in regions with ‘neural reserve', where cortical responses to visual stimulation do not lead to visual awareness as assessed by Humphrey perimetry—a standard behavioural visual field test. Here, we tested this hypothesis in a sample of twenty-seven hemianopic stroke patients, who participated in an assiduous 80-hour VRT program. For each patient, we collected Humphrey perimetry and wide-field fMRI-based retinotopic mapping data prior to training. In addition, we used Goal Attainment Scaling to assess whether personal activities in daily living improved. After training, we assessed with a second Humphrey perimetry measurement whether the visual field was improved and evaluated which personal goals were attained. Confirming the hypothesis, we found significantly larger improvements of visual sensitivity at field locations with neural reserve. These visual field improvements implicated both regions in primary visual cortex and higher order visual areas. In addition, improvement in daily life activities correlated with the extent of visual field enlargement. Our findings are an important step toward understanding the mechanisms of visual restitution as well as predicting training efficacy in stroke patients with chronic hemianopia.
Farzad V. Farahani; Magdalena Fafrowicz; Waldemar Karwowski; Bartosz Bohaterewicz; Anna Maria Sobczak; Anna Ceglarek; Aleksandra Zyrkowska; Monika Ostrogorska; Barbara Sikora-Wachowicz; Koryna Lewandowska; Halszka Oginska; Anna Beres; Magdalena Hubalewska-Mazgaj; Tadeusz Marek
Identifying diurnal variability of brain connectivity patterns using graph theory Journal Article
In: Brain Sciences, vol. 11, no. 1, pp. 111, 2021.
Significant differences exist in human brain functions affected by time of day and by people's diurnal preferences (chronotypes) that are rarely considered in brain studies. In the current study, using network neuroscience and resting-state functional MRI (rs-fMRI) data, we examined the effect of both time of day and the individual's chronotype on whole-brain network organization. In this regard, 62 participants (39 women; mean age: 23.97 ± 3.26 years; half morning-versus half evening-type) were scanned about 1 and 10 h after wake-up time for morning and evening sessions, respectively. We found evidence for a time-of-day effect on connectivity profiles but not for the effect of chronotype. Compared with the morning session, we found relatively higher small-worldness (an index that represents more efficient network organization) in the evening session, which suggests the dominance of sleep inertia over the circadian and homeostatic processes in the first hours after waking. Furthermore, local graph measures were changed, predominantly across the left hemisphere, in areas such as the precentral gyrus, putamen, inferior frontal gyrus (orbital part), inferior temporal gyrus, as well as the bilateral cerebellum. These findings show the variability of the functional neural network architecture during the day and improve our understanding of the role of time of day in resting-state functional networks.
Emily S. Finn; Peter A. Bandettini
Movie-watching outperforms rest for functional connectivity-based prediction of behavior Journal Article
In: NeuroImage, vol. 235, pp. 117963, 2021.
A major goal of human neuroscience is to relate differences in brain function to differences in behavior across people. Recent work has established that whole-brain functional connectivity patterns are relatively stable within individuals and unique across individuals, and that features of these patterns predict various traits. However, while functional connectivity is most often measured at rest, certain tasks may enhance individual signals and improve sensitivity to behavior differences. Here, we show that compared to the resting state, functional connectivity measured during naturalistic viewing—i.e., movie watching—yields more accurate predictions of trait-like phenotypes in the domains of both cognition and emotion. Traits could be predicted using less than three minutes of data from single video clips, and clips with highly social content gave the most accurate predictions. Results suggest that naturalistic stimuli amplify individual differences in behaviorally relevant brain networks.
Markus Frey; Matthias Nau; Christian F. Doeller
Magnetic resonance-based eye tracking using deep neural networks Journal Article
In: Nature Neuroscience, vol. 24, no. 12, pp. 1772–1779, 2021.
Viewing behavior provides a window into many central aspects of human cognition and health, and it is an important variable of interest or confound in many functional magnetic resonance imaging (fMRI) studies. To make eye tracking freely and widely available for MRI research, we developed DeepMReye, a convolutional neural network (CNN) that decodes gaze position from the magnetic resonance signal of the eyeballs. It performs cameraless eye tracking at subimaging temporal resolution in held-out participants with little training data and across a broad range of scanning protocols. Critically, it works even in existing datasets and when the eyes are closed. Decoded eye movements explain network-wide brain activity also in regions not associated with oculomotor function. This work emphasizes the importance of eye tracking for the interpretation of fMRI results and provides an open source software solution that is widely applicable in research and clinical settings.
Esther Fujiwara; Christopher R. Madan; Jeremy B. Caplan; Tobias Sommer
Emotional arousal impairs association memory: Roles of prefrontal cortex regions Journal Article
In: Learning and Memory, vol. 28, no. 3, pp. 76–81, 2021.
The brain processes underlying impairing effects of emotional arousal on associative memory were previously attributed to two dissociable routes using high-resolution fMRI of the MTL (Madan et al. 2017). Extrahippocampal MTL regions supporting associative encoding of neutral pairs suggested unitization; conversely, associative encoding of negative pairs involved compensatory hippocampal activity. Here, whole-brain fMRI revealed prefrontal contributions: dmPFC was more involved in hippocampal-dependent negative pair learning and vmPFC in extrahippocampal neutral pair learning. Successful encoding of emotional memory associations may require emotion regulation/conflict resolution (dmPFC), while neutral memory associations may be accomplished by anchoring new information to prior knowledge (vmPFC).
Max Garagnani; Evgeniya Kirilina; Friedemann Pulvermüller
Semantic grounding of novel spoken words in the primary visual cortex Journal Article
In: Frontiers in Human Neuroscience, vol. 15, pp. 1–16, 2021.
Embodied theories of grounded semantics postulate that, when word meaning is first acquired, a link is established between symbol (word form) and corresponding semantic information present in modality-specific—including primary—sensorimotor cortices of the brain. Direct experimental evidence documenting the emergence of such a link (i.e., showing that presentation of a previously unknown, meaningless word sound induces, after learning, category-specific reactivation of relevant primary sensory or motor brain areas), however, is still missing. Here, we present new neuroimaging results that provide such evidence. We taught participants aspects of the referential meaning of previously unknown, senseless novel spoken words (such as “Shruba” or “Flipe”) by associating them with either a familiar action or a familiar object. After training, we used functional magnetic resonance imaging to analyze the participants' brain responses to the new speech items. We found that hearing the newly learnt object-related word sounds selectively triggered activity in the primary visual cortex, as well as secondary and higher visual areas.These results for the first time directly document the formation of a link between the novel, previously meaningless spoken items and corresponding semantic information in primary sensory areas in a category-specific manner, providing experimental support for perceptual accounts of word-meaning acquisition in the brain.
Kyle M. Gilbert; L. Martyn Klassen; Alexander Mashkovtsev; Peter Zeman; Ravi S. Menon; Joseph S. Gati
Radiofrequency coil for routine ultra-high-field imaging with an unobstructed visual field Journal Article
In: NMR in Biomedicine, vol. 34, no. 3, pp. e4457, 2021.
Many neuroscience applications have adopted functional MRI as a tool to investigate the healthy and diseased brain during the completion of a task. While ultra-high-field MRI has allowed for improved contrast and signal-to-noise ratios during functional MRI studies, it remains a challenge to create local radiofrequency coils that can accommodate an unobstructed visual field and be suitable for routine use, while at the same time not compromise performance. Performance (both during transmission and reception) can be improved by using close-fitting coils; however, maintaining sensitivity over the whole brain often requires the introduction of coil elements proximal to the eyes, thereby partially occluding the subject's visual field. This study presents a 7 T head coil, with eight transmit dipoles and 32 receive loops, that is designed to remove visual obstructions from the subject's line of sight, allowing for an unencumbered view of visual stimuli, the reduction of anxiety induced from small enclosures, and the potential for eye-tracking measurements. The coil provides a practical solution for routine imaging, including a split design (anterior and posterior halves) that facilitates subject positioning, including those with impaired mobility, and the placement of devices required for patient comfort and motion reduction. The transmit and receive coils displayed no degradation of performance due to adaptions to the design topology (both mechanical and electrical) required to create an unobstructed visual field. All computer-aided design files, electromagnetic simulation models, transmit field maps and local specific absorption rate matrices are provided to promote reproduction.
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.
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.
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.
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.
Hinke N. Halbertsma; Holly Bridge; Joana Carvalho; Frans W. Cornelissen; Sara Ajina
Visual field reconstruction in hemianopia using fMRI based mapping techniques Journal Article
In: Frontiers in Human Neuroscience, vol. 15, pp. 713114, 2021.
Purpose: A stroke that includes the primary visual cortex unilaterally leads to a loss of visual field (VF) representation in the hemifield contralateral to the damage. While behavioral procedures for measuring the VF, such as perimetry, may indicate that a patient cannot see in a particular area, detailed psychophysical testing often detects the ability to perform detection or discrimination of visual stimuli (“blindsight”). The aim of this study was to determine whether functional magnetic resonance imaging (fMRI) could be used to determine whether perimetrically blind regions of the VF were still represented in VF maps reconstructed on the basis of visually evoked neural activity. Methods: Thirteen patients with hemianopia and nine control participants were scanned using 3T MRI while presented with visual stimulation. Two runs of a dynamic “wedge and ring” mapping stimulus, totaling approximately 10 min, were performed while participants fixated centrally. Two different analysis approaches were taken: the conventional population receptive field (pRF) analysis and micro-probing (MP). The latter is a variant of the former that makes fewer assumptions when modeling the visually evoked neural activity. Both methods were used to reconstruct the VF by projecting modeled activity back onto the VF. Following a normalization step, these “coverage maps” can be compared to the VF sensitivity plots obtained using perimetry. Results: While both fMRI-based approaches revealed regions of neural activity within the perimetrically “blind” sections of the VF, the MP approach uncovered more voxels in the lesioned hemisphere in which a modest degree of visual sensitivity was retained. Furthermore, MP-based analysis indicated that both early (V1/V2) and extrastriate visual areas contributed equally to the retained sensitivity in both patients and controls. Conclusion: In hemianopic patients, fMRI-based approaches for reconstructing the VF can pick up activity in perimetrically blind regions of the VF. Such regions of the VF may be particularly amenable for rehabilitation to regain visual function. Compared to conventional pRF modeling, MP reveals more voxels with retained visual sensitivity, suggesting it is a more sensitive approach for VF reconstruction.
Grace E. Hallenbeck; Thomas C. Sprague; Masih Rahmati; Kartik K. Sreenivasan; Clayton E. Curtis
Working memory representations in visual cortex mediate distraction effects Journal Article
In: Nature Communications, vol. 12, pp. 4714, 2021.
Although the contents of working memory can be decoded from visual cortex activity, these representations may play a limited role if they are not robust to distraction. We used model-based fMRI to estimate the impact of distracting visual tasks on working memory representations in several visual field maps in visual and frontoparietal association cortex. Here, we show distraction causes the fidelity of working memory representations to briefly dip when both the memorandum and distractor are jointly encoded by the population activities. Distraction induces small biases in memory errors which can be predicted by biases in neural decoding in early visual cortex, but not other regions. Although distraction briefly disrupts working memory representations, the widespread redundancy with which working memory information is encoded may protect against catastrophic loss. In early visual cortex, the neural representation of information in working memory and behavioral performance are intertwined, solidifying its importance in visual memory.
Anja Ischebeck; Hannah Hiebel; Joe Miller; Margit Höfler; Iain D. Gilchrist; Christof Körner
Target processing in overt serial visual search involves the dorsal attention network: A fixation-based event-related fMRI study Journal Article
In: Neuropsychologia, vol. 153, pp. 107763, 2021.
In serial visual search we shift attention successively from location to location in search for the target. Although such search has been investigated using fMRI, overt attention (i.e., eye movements) was usually neglected or discouraged. As a result, it is unclear what happens in the instant when our gaze falls upon a target as compared to a distractor. In the present experiment, we used a multiple target search task that required eye movements and employed an analysis based on fixations as events of interest to investigate differences between target and distractor processing. Twenty young healthy adults indicated the number of targets (0–3) among distractors in a 20-item display. Compared to distractor fixations, we found that target fixations gave rise to wide-spread activation in the dorsal attention system, as well as in the visual cortex. Targets that were found later during the search activated the left inferior frontal gyrus and the left supramarginal gyrus more strongly than those that were found earlier. Finally, areas associated with visual and verbal working memory showed increased activation with a larger number of targets in the display.
Joonyoung Kang; Hyeji Kim; Seong Hwan Hwang; Minjun Han; Sue-Hyun Lee; Hyoung F. Kim
Primate ventral striatum maintains neural representations of the value of previously rewarded objects for habitual seeking Journal Article
In: Nature Communications, vol. 12, pp. 2100, 2021.
The ventral striatum (VS) is considered a key region that flexibly updates recent changes in reward values for habit learning. However, this update process may not serve to maintain learned habitual behaviors, which are insensitive to value changes. Here, using fMRI in humans and single-unit electrophysiology in macaque monkeys we report another role of the primate VS: that the value memory subserving habitual seeking is stably maintained in the VS. Days after object-value associative learning, human and monkey VS continue to show increased responses to previously rewarded objects, even when no immediate reward outcomes are expected. The similarity of neural response patterns to each rewarded object increases after learning among participants who display habitual seeking. Our data show that long-term memory of high-valued objects is retained as a single representation in the VS and may be utilized to evaluate visual stimuli automatically to guide habitual behavior.
Sabrina Karl; Ronald Sladky; Claus Lamm; Ludwig Huber
Neural responses of pet dogs witnessing their caregiver's positive interactions with a conspecific: An fMRI study Journal Article
In: Cerebral Cortex Communications, vol. 2, no. 3, pp. tgab047, 2021.
We have limited knowledge on how dogs perceive humans and their actions. Various researchers investigated how they process human facial expressions, but their brain responses to complex social scenarios remain unclear. While undergoing fMRI, we exposed pet dogs to videos showing positive social and neutral nonsocial interactions between their caregivers and another conspecific. Our main interest was how the dogs responded to their caregivers (compared to a stranger) engaging in a pleasant interaction with another dog that could be seen as social rival. We hypothesized that the dogs would show activation increases in limbic areas such as the amygdala, hypothalamus, and insula and likely show higher attention and arousal during the positive caregiver–dog interaction. When contrasting the social with the nonsocial interaction, we found increased activations in the left amygdala and the insular cortex. Crucially, the dogs' hypothalamus showed strongest activation when the caregiver engaged in a positive social interaction. These findings indicate that dogs are sensitive to social affective human–dog interactions and likely show higher valence attribution and arousal in a situation possibly perceived as a potential threat to their caregiver bonds. Our study provides a first window into the neural correlates of social and emotional processing in dogs.
Haena Kim; Namrata Nanavaty; Humza Ahmed; Vani A. Mathur; Brian A. Anderson
Motivational salience guides attention to valuable and threatening stimuli: Evidence from behavior and functional magnetic resonance imaging Journal Article
In: Journal of Cognitive Neuroscience, vol. 33, no. 12, pp. 2440–2460, 2021.
Rewarding and aversive outcomes have opposing effects on behavior, facilitating approach and avoidance, although we need to accurately anticipate each type of outcome to behave effectively. Attention is biased toward stimuli that have been learned to predict either type of outcome, and it remains an open question whether such orienting is driven by separate systems for value-and threat-based orienting or whether there exists a common underlying mechanism of attentional control driven by motivational salience. Here, we provide a direct comparison of the neural correlates of value-and threat-based attentional capture after associative learning. Across multiple measures of behavior and brain activation, our findings overwhelmingly support a motivational salience account of the control of attention. We conclude that there exists a core mechanism of experience-dependent attentional control driven by motivational salience and that prior characterizations of attention as being value driven or supporting threat monitoring need to be revisited.
Na Yeon Kim; Mark A. Pinsk; Sabine Kastner
Neural basis of biased competition in development: sensory competition in visual cortex of school-aged children Journal Article
In: Cerebral Cortex, vol. 31, no. 6, pp. 3107–3121, 2021.
The fundamental receptive field (RF) architecture in human visual cortex becomes adult-like by age 5. However, visuo-spatial functions continue to develop until teenage years. This suggests that, despite the early maturation of the RF structure, functional interactions within and across RFs may mature slowly. Here, we used fMRI to investigate functional interactions among multiple stimuli in the visual cortex of school children (ages 8 to 12) in the context of biased competition theory. In the adult visual system, multiple objects presented in the same visual field compete for neural representation. These competitive interactions occur at the level of the RF and are therefore closely linked to the RF architecture. Like in adults, we found suppression of evoked responses in children's visual cortex when multiple stimuli were presented simultaneously. Such suppression effects were modulated by the spatial distance between the stimuli as a function of RF size across the visual system. Our findings suggest that basic competitive interactions in the visual cortex of children above age 8 operate in an adult-like manner, with subtle differences in early visual areas and area MT. Our study establishes a paradigm and provides baseline data to investigate the neural basis of visuo-spatial processing in typical and atypical development.
Florian Krause; Nikos Kogias; Martin Krentz; Michael Lührs; Rainer Goebel; Erno J. Hermans
Self-regulation of stress-related large-scale brain network balance using real-time fMRI neurofeedback Journal Article
In: NeuroImage, vol. 243, pp. 118527, 2021.
It has recently been shown that acute stress affects the allocation of neural resources between large-scale brain networks, and the balance between the executive control network and the salience network in particular. Maladaptation of this dynamic resource reallocation process is thought to play a major role in stress-related psychopathology, suggesting that stress resilience may be determined by the retained ability to adaptively reallocate neural resources between these two networks. Actively training this ability could hence be a potentially promising way to increase resilience in individuals at risk for developing stress-related symptomatology. Using real-time functional Magnetic Resonance Imaging, the current study investigated whether individuals can learn to self-regulate stress-related large-scale network balance. Participants were engaged in a bidirectional and implicit real-time fMRI neurofeedback paradigm in which they were intermittently provided with a visual representation of the difference signal between the average activation of the salience and executive control networks, and tasked with attempting to self-regulate this signal. Our results show that, given feedback about their performance over three training sessions, participants were able to (1) learn strategies to differentially control the balance between SN and ECN activation on demand, as well as (2) successfully transfer this newly learned skill to a situation where they (a) did not receive any feedback anymore, and (b) were exposed to an acute stressor in form of the prospect of a mild electric stimulation. The current study hence constitutes an important first successful demonstration of neurofeedback training based on stress-related large-scale network balance – a novel approach that has the potential to train control over the central response to stressors in real-life and could build the foundation for future clinical interventions that aim at increasing resilience.
Irma T. Kurniawan; Marcus Grueschow; Christian C. Ruff
Anticipatory energization revealed by pupil and brain activity guides human effort-based decision making Journal Article
In: Journal of Neuroscience, vol. 41, no. 29, pp. 6328–6342, 2021.
An organism's fitness is determined by how it chooses to adapt to effort in response to challenges. Exertion of effort correlates with activity in dorsomedial prefrontal cortex (dmPFC) and noradrenergic pupil dilation, but little is known about the role of these neurophysiological processes for decisions about future efforts, they may provide anticipatory energization to help us accept the challenge or a cost representation that is weighted against the expected rewards. Here, we provide evidence for the former, by measuring pupil and functional magnetic resonance imaging (fMRI) brain responses while 52 human participants (29 females) chose whether to exert efforts to obtain rewards. Both pupil-dilation rate and dmPFC fMRI activity increased with anticipated effort level, and these increases differ depending on the choice outcome: they were stronger when participants chose to accept the challenge compared with when the challenge was declined. Crucially, the choice-dependent modulation of pupil and brain-activity effort representations were stronger in participants whose behavioral choices were more sensitive to effort. Our results identify a process involving the peripheral and central human nervous system that simulates the required energization before overt response, suggesting a role in guiding effort-based decisions.
Hsin-Hung Li; Thomas C. Sprague; Aspen H. Yoo; Wei Ji Ma; Clayton E. Curtis
Joint representation of working memory and uncertainty in human cortex Journal Article
In: Neuron, vol. 109, no. 22, pp. 3699–3712, 2021.
Neural representations of visual working memory (VWM) are noisy, and thus, decisions based on VWM are inevitably subject to uncertainty. However, the mechanisms by which the brain simultaneously represents the content and uncertainty of memory remain largely unknown. Here, inspired by the theory of probabilistic population codes, we test the hypothesis that the human brain represents an item maintained in VWM as a probability distribution over stimulus feature space, thereby capturing both its content and uncertainty. We used a neural generative model to decode probability distributions over memorized locations from fMRI activation patterns. We found that the mean of the probability distribution decoded from retinotopic cortical areas predicted memory reports on a trial-by-trial basis. Moreover, in several of the same mid-dorsal stream areas, the spread of the distribution predicted subjective trial-by-trial uncertainty judgments. These results provide evidence that VWM content and uncertainty are jointly represented by probabilistic neural codes.
Björn Machner; Jonathan Imholz; Lara Braun; Philipp J. Koch; Tobias Bäumer; Thomas F. Münte; Christoph Helmchen; Andreas Sprenger
Resting-state functional connectivity in the attention networks is not altered by offline theta-burst stimulation of the posterior parietal cortex or the temporo-parietal junction as compared to a vertex control site Journal Article
In: Neuroimage: Reports, vol. 1, no. 2, pp. 100013, 2021.
Disruption of resting-state functional connectivity (RSFC) between core regions of the dorsal attention network (DAN), including the bilateral superior parietal lobule (SPL), and structural damage of the right-lateralized ventral attention network (VAN), including the temporo-parietal junction (TPJ), have been described as neural basis for hemispatial neglect. Pursuing a virtual lesion model, we aimed to perturbate the attention networks of 22 healthy subjects by applying continuous theta burst stimulation (cTBS) to the right SPL or TPJ. We first created network masks of the DAN and VAN based on RSFC analyses from a RS-fMRI baseline session and determined the SPL and TPJ stimulation site within the respective mask. We then performed RS-fMRI immediately after cTBS of the SPL, TPJ (active sites) or vertex (control site). RSFC between SPL/TPJ and whole brain as well as between predefined regions of interest (ROI) in the attention networks was analyzed in a within-subject design. Contrary to our hypothesis, seed-based RSFC did not differ between the four experimental conditions. The individual change in ROI-to-ROI RSFC from baseline to post-stimulation did also not differ between active (SPL, TPJ) and control (vertex) cTBS. In our study, a single session offline cTBS over the right SPL or TPJ could not alter RSFC in the attention networks as compared to a control stimulation, maybe because effects wore off too early. Future studies should consider a modified cTBS protocol, concurrent TMS-fMRI or transcranial direct current stimulation.
Jennifer E. Mack; Colleen Ward; Sofia Stratford
Impact of the fMRI environment on eye-tracking measures in a linguistic prediction task Journal Article
In: Language, Cognition and Neuroscience, vol. 36, no. 6, pp. 675–693, 2021.
The present study investigated the impact of the MRI environment on eye-movement measures in the visual-world paradigm. 24 neurotypical young adults performed a linguistic prediction task in a typical lab setting (Lab) and 22 did so during MRI scanning (Scanner). Data analyses focused on eye-tracking data quality and the time course and magnitude of prediction effects. Data quality was reduced in the Scanner as compared to the Lab, as indicated by a higher rate of track loss and saccades/fixations of atypical duration. Predictive eye movement patterns were generally similar in timing and magnitude between the Lab and Scanner, although there was modest evidence for increased prediction effects in the Scanner. In the Scanner environment only, predictive eye movements were linked to better task performance. Evidently, the MRI environment can enhance prediction effects and their relationship to task performance, possibly due to increased deployment of cognitive control mechanisms.
Pupil-based states of brain integration across cognitive states Journal Article
In: Neuroscience, vol. 471, pp. 61–71, 2021.
Arousal is a potent mechanism that provides the brain with functional flexibility and adaptability to external conditions. Within the wake state, arousal levels driven by activity in the neuromodulatory systems are related to specific signatures of neural activation and brain synchrony. However, direct evidence is still lacking on the varying effects of arousal on macroscopic brain characteristics and across a variety of cognitive states in humans. Using a concurrent fMRI-pupillometry approach, we used pupil size as a proxy for arousal and obtained patterns of brain integration associated with increasing arousal levels. We carried out this analysis on resting-state data and data from two attentional tasks implicating different cognitive processes. We found that an increasing level of arousal was related to a state of increased brain integration. This effect was prominent in the salience, visual and default-mode networks in all conditions, while other regions showed task-specificity. Increased integration in the salience network was also related to faster pupil dilation in the two attentional tasks. Furthermore, task performance was related to arousal level, with lower accuracy at higher level of arousal. Taken together, our study provides evidence in humans for pupil size as an index of brain network state, and supports the role of arousal as a switch that drives brain coordination in specific brain regions according to the cognitive state.
Cornelia McCormick; Marshall A. Dalton; Peter Zeidman; Eleanor A. Maguire
Characterising the hippocampal response to perception, construction and complexity Journal Article
In: Cortex, vol. 137, pp. 1–17, 2021.
The precise role played by the hippocampus in supporting cognitive functions such as episodic memory and future thinking is debated, but there is general agreement that it involves constructing representations comprised of numerous elements. Visual scenes have been deployed extensively in cognitive neuroscience because they are paradigmatic multi-element stimuli. However, questions remain about the specificity and nature of the hippocampal response to scenes. Here, we devised a paradigm in which we had participants search pairs of images for either colour or layout differences, thought to be associated with perceptual or spatial constructive processes respectively. Importantly, images depicted either naturalistic scenes or phase-scrambled versions of the same scenes, and were either simple or complex. Using this paradigm during functional MRI scanning, we addressed three questions: 1. Is the hippocampus recruited specifically during scene processing? 2. If the hippocampus is more active in response to scenes, does searching for colour or layout differences influence its activation? 3. Does the complexity of the scenes affect its response? We found that, compared to phase-scrambled versions of the scenes, the hippocampus was more responsive to scene stimuli. Moreover, a clear anatomical distinction was evident, with colour detection in scenes engaging the posterior hippocampus whereas layout detection in scenes recruited the anterior hippocampus. The complexity of the scenes did not influence hippocampal activity. These findings seem to align with perspectives that propose the hippocampus is especially attuned to scenes, and its involvement occurs irrespective of the cognitive process or the complexity of the scenes.
Cornelia McCormick; Eleanor A. Maguire
The distinct and overlapping brain networks supporting semantic and spatial constructive scene processing Journal Article
In: Neuropsychologia, vol. 158, pp. 107912, 2021.
Scene imagery features prominently when we recall autobiographical memories, imagine the future and navigate around in the world. Consequently, in this study we sought to better understand how scene representations are supported by the brain. Processing scenes involves a variety of cognitive processes that in the real world are highly interactive. Here, however, our goal was to separate semantic and spatial constructive scene processes in order to identify the brain areas that were distinct to each process, those they had in common, and the connectivity between regions. To this end, participants searched for either semantic or spatial constructive impossibilities in scenes during functional MRI. We focussed our analyses on only those scenes that were possible, thus removing any error detection that would evoke reactions such as surprise or novelty. Importantly, we also counterbalanced possible scenes across participants, enabling us to examine brain activity and connectivity for the same possible scene images under two different conditions. We found that participants adopted different cognitive strategies, which were reflected in distinct oculomotor behaviour, for each condition. These were in turn associated with increased engagement of lateral temporal and parietal cortices for semantic scene processing, the hippocampus for spatial constructive scene processing, and increased activation of the ventromedial prefrontal cortex (vmPFC) that was common to both. Connectivity analyses showed that the vmPFC switched between semantic and spatial constructive brain networks depending on the task at hand. These findings further highlight the well-known semantic functions of lateral temporal areas, while providing additional support for the previously-asserted contribution of the hippocampus to scene construction, and recent suggestions that the vmPFC may play a key role in orchestrating scene processing.
Sreenivasan Meyyappan; Abhijit Rajan; George R. Mangun; Mingzhou Ding
Role of inferior frontal junction (IFJ) in the control of feature versus spatial attention Journal Article
In: Journal of Neuroscience, vol. 41, no. 38, pp. 8065–8074, 2021.
Feature-based visual attention refers to preferential selection and processing of visual stimuli based on their nonspatial attributes, such as color or shape. Recent studies have highlighted the inferior frontal junction (IFJ) as a control region for feature but not spatial attention. However, the extent to which IFJ contributes to spatial versus feature attention control remains a topic of debate. We investigated in humans of both sexes the role of IFJ in the control of feature versus spatial attention in a cued visual spatial (attend-left or attend-right) and feature (attend-red or attend-green) attention task using fMRI. Analyzing cue-related fMRI using both univariate activation and multivoxel pattern analysis, we found the following results in IFJ. First, in line with some prior studies, the univariate activations were not different between feature and spatial attentional control. Second, in contrast, the multivoxel pattern analysis decoding accuracy was above chance level for feature attention (attend-red vs attend-green) but not for spatial attention (attend-left vs attend-right). Third, while the decoding accuracy for feature attention was above chance level during attentional control in the cue-to-target interval, it was not during target processing. Fourth, the right IFJ and visual cortex (V4) were observed to be functionally connected during feature but not during spatial attention control, and this functional connectivity was positively associated with subsequent attentional selection of targets in V4, as well as with behavioral performance. These results support a model in which IFJ plays a crucial role in topdown control of visual feature but not visual spatial attention.
Kentaro Miyamoto; Nadescha Trudel; Kevin Kamermans; Michele C. Lim; Alberto Lazari; Lennart Verhagen; Marco K. Wittmann; Matthew F. S. Rushworth
Identification and disruption of a neural mechanism for accumulating prospective metacognitive information prior to decision-making Journal Article
In: Neuron, vol. 109, no. 8, pp. 1396–1408, 2021.
More than one type of probability must be considered when making decisions. It is as necessary to know one's chance of performing choices correctly as it is to know the chances that desired outcomes will follow choices. We refer to these two choice contingencies as internal and external probability. Neural activity across many frontal and parietal areas reflected internal and external probabilities in a similar manner during decision-making. However, neural recording and manipulation approaches suggest that one area, the anterior lateral prefrontal cortex (alPFC), is highly specialized for making prospective, metacognitive judgments on the basis of internal probability; it is essential for knowing which decisions to tackle, given its assessment of how well they will be performed. Its activity predicted prospective metacognitive judgments, and individual variation in activity predicted individual variation in metacognitive judgments. Its disruption altered metacognitive judgments, leading participants to tackle perceptual decisions they were likely to fail.
Viola Mocz; Maryam Vaziri-Pashkam; Marvin Chun; Yaoda Xu
Predicting identity-preserving object transformations across the human ventral visual stream Journal Article
In: Journal of Neuroscience, vol. 41, no. 35, pp. 7403–7419, 2021.
In everyday life, we have no trouble categorizing objects varying in position, size, and orientation. Previous fMRI research shows that higher-level object processing regions in the human lateral occipital cortex may link object responses from different affine states (i.e. size and viewpoint) through a general linear mapping function capable of predicting responses to novel objects. In this study, we extended this approach to examine the mapping for both Euclidean (e.g. position and size) and non-Euclidean (e.g. image statistics and spatial frequency) transformations across the human ventral visual processing hierarchy, including areas V1, V2, V3, V4, ventral occipitotemporal cortex (VOT), and lateral occipitotemporal cortex (LOT). The predicted pattern generated from a linear mapping function could capture a significant amount of the changes associated with the transformations throughout the ventral visual stream. The derived linear mapping functions were not category independent, as performance was better for the categories included than those not included in training and better between two similar versus two dissimilar categories in both lower and higher visual regions. Consistent with object representations being stronger in higher than lower visual regions, pattern selectivity and object category representational structure were somewhat better preserved in the predicted patterns in higher than lower visual regions. There were no notable differences between Euclidean and non-Euclidean transformations. These findings demonstrate a near-orthogonal representation of object identity and these non-identity features throughout the human ventral visual processing pathway, with these non-identity features largely untangled from the identity features early in visual processing.
Tianlu Wang; Lena M. Hofbauer; Dante Mantini; Céline R. Gillebert
Behavioural and neural effects of eccentricity and visual field during covert visuospatial attention Journal Article
In: Neuroimage: Reports, vol. 1, no. 3, pp. 100039, 2021.
The attentional priority map plays a key role in the distribution of attention, and is modulated by bottom-up sensory as well as top-down task-dependent factors. The intraparietal sulcus (IPS) is a key candidate to hold a neural representation of the attentional priority map. In the current study, we examined the role of the IPS during covert attention to spatial locations with high or low eccentricity in one or both visual hemifields. To this end, eighteen neurologically healthy participants performed a cued letter discrimination task in which they were endogenously cued to attend to a location at a 5 or 10◦ eccentricity in the left and/or right visual field. We briefly presented a four-letter target array and subsequently probed perceptual performance while acquiring event- related functional MRI data. While behavioural results showed greater letter discrimination performance at the low eccentricity compared to the high eccentricity location, no neural effect of eccentricity was observed. The results further showed that attending to one visual hemifield produced higher activation in the left parietal and occipital cortex compared to attending bilaterally. Future studies may consider increasing the involvement of top-down control of attention to the cued location to study the neural effect of eccentricity, e.g., through manipulating the task difficulty.
Bo Yao; Jason R. Taylor; Briony Banks; Sonja A. Kotz
Reading direct speech quotes increases theta phase-locking: Evidence for cortical tracking of inner speech? Journal Article
In: NeuroImage, vol. 239, pp. 118313, 2021.
Growing evidence shows that theta-band (4–7 Hz) activity in the auditory cortex phase-locks to rhythms of overt speech. Does theta activity also encode the rhythmic dynamics of inner speech? Previous research established that silent reading of direct speech quotes (e.g., Mary said: “This dress is lovely!”) elicits more vivid inner speech than indirect speech quotes (e.g., Mary said that the dress was lovely). As we cannot directly track the phase alignment between theta activity and inner speech over time, we used EEG to measure the brain's phase-locked responses to the onset of speech quote reading. We found that direct (vs. indirect) quote reading was associated with increased theta phase synchrony over trials at 250–500 ms post-reading onset, with sources of the evoked activity estimated in the speech processing network. An eye-tracking control experiment confirmed that increased theta phase synchrony in direct quote reading was not driven by eye movement patterns, and more likely reflects synchronous phase resetting at the onset of inner speech. These findings suggest a functional role of theta phase modulation in reading-induced inner speech.
Nicole H. Yuen; Fred Tam; Nathan W. Churchill; Tom A. Schweizer; Simon J. Graham
Driving with distraction: Measuring brain activity and oculomotor behavior using fMRI and eye-tracking Journal Article
In: Frontiers in Human Neuroscience, vol. 15, pp. 1–20, 2021.
Introduction: Driving motor vehicles is a complex task that depends heavily on how visual stimuli are received and subsequently processed by the brain. The potential impact of distraction on driving performance is well known and poses a safety concern – especially for individuals with cognitive impairments who may be clinically unfit to drive. The present study is the first to combine functional magnetic resonance imaging (fMRI) and eye-tracking during simulated driving with distraction, providing oculomotor metrics to enhance scientific understanding of the brain activity that supports driving performance. Materials and Methods: As initial work, twelve healthy young, right-handed participants performed turns ranging in complexity, including simple right and left turns without oncoming traffic, and left turns with oncoming traffic. Distraction was introduced as an auditory task during straight driving, and during left turns with oncoming traffic. Eye-tracking data were recorded during fMRI to characterize fixations, saccades, pupil diameter and blink rate. Results: Brain activation maps for right turns, left turns without oncoming traffic, left turns with oncoming traffic, and the distraction conditions were largely consistent with previous literature reporting the neural correlates of simulated driving. When the effects of distraction were evaluated for left turns with oncoming traffic, increased activation was observed in areas involved in executive function (e.g., middle and inferior frontal gyri) as well as decreased activation in the posterior brain (e.g., middle and superior occipital gyri). Whereas driving performance remained mostly unchanged (e.g., turn speed, time to turn, collisions), the oculomotor measures showed that distraction resulted in more consistent gaze at oncoming traffic in a small area of the visual scene; less time spent gazing at off-road targets (e.g., speedometer, rear-view mirror); more time spent performing saccadic eye movements; and decreased blink rate. Conclusion: Oculomotor behavior modulated with driving task complexity and distraction in a manner consistent with the brain activation features revealed by fMRI. The results suggest that eye-tracking technology should be included in future fMRI studies of simulated driving behavior in targeted populations, such as the elderly and individuals with cognitive complaints – ultimately toward developing better technology to assess and enhance fitness to drive.
Shengnan Zhu; Yang Zhang; Junli Dong; Lihong Chen; Wenbo Luo
Low-spatial-frequency information facilitates threat detection in a response-specific manner Journal Article
In: Journal of Vision, vol. 21, no. 4, pp. 1–9, 2021.
The role of different spatial frequency bands in threat detection has been explored extensively. However, most studies use manual responses and the results are mixed. Here, we aimed to investigate the contribution of spatial frequency information to threat detection by using three response types, including manual responses, eye movements, and reaching movements, together with a priming paradigm. The results showed that both saccade and reaching responses were significantly faster to threatening stimuli than to nonthreatening stimuli when primed by low-spatial-frequency gratings rather than by high-spatial-frequency gratings. However, the manual response times to threatening stimuli were comparable to nonthreatening stimuli, irrespective of the spatial frequency content of the primes. The findings provide clear evidence that low-spatial-frequency information can facilitate threat detection in a response-specific manner, possibly through the subcortical magnocellular pathway dedicated to processing threat-related signals, which is automatically prioritized in the oculomotor system and biases behavior.
Kristin Marie Zimmermann; Kirsten Daniela Schmidt; Franziska Gronow; Jens Sommer; Frank Leweke; Andreas Jansen
Seeing things differently: Gaze shapes neural signal during mentalizing according to emotional awareness Journal Article
In: NeuroImage, vol. 238, pp. 1–14, 2021.
Studies on social cognition often use complex visual stimuli to asses neural processes attributed to abilities like “mentalizing” or “Theory of Mind” (ToM). During the processing of these stimuli, eye gaze, however, shapes neural signal patterns. Individual differences in neural operations on social cognition may therefore be obscured if individuals' gaze behavior differs systematically. These obstacles can be overcome by the combined analysis of neural signal and natural viewing behavior. Here, we combined functional magnetic resonance imaging (fMRI) with eye-tracking to examine effects of unconstrained gaze on neural ToM processes in healthy individuals with differing levels of emotional awareness, i.e. alexithymia. First, as previously described for emotional tasks, people with higher alexithymia levels look less at eyes in both ToM and task-free viewing contexts. Further, we find that neural ToM processes are not affected by individual differences in alexithymia per se. Instead, depending on alexithymia levels, gaze on critical stimulus aspects reversely shapes the signal in medial prefrontal cortex (MPFC) and anterior temporoparietal junction (TPJ) as distinct nodes of the ToM system. These results emphasize that natural selective attention affects fMRI patterns well beyond the visual system. Our study implies that, whenever using a task with multiple degrees of freedom in scan paths, ignoring the latter might obscure important conclusions.
Fosca Al Roumi; Sébastien Marti; Liping Wang; Marie Amalric; Stanislas Dehaene
Mental compression of spatial sequences in human working memory using numerical and geometrical primitives Journal Article
In: Neuron, vol. 109, no. 16, pp. 2627–2639, 2021.
How does the human brain store sequences of spatial locations? We propose that each sequence is internally compressed using an abstract, language-like code that captures its numerical and geometrical regularities. We exposed participants to spatial sequences of fixed length but variable regularity while their brain activity was recorded using magneto-encephalography. Using multivariate decoders, each successive location could be decoded from brain signals, and upcoming locations were anticipated prior to their actual onset. Crucially, sequences with lower complexity, defined as the minimal description length provided by the formal language, led to lower error rates and to increased anticipations. Furthermore, neural codes specific to the numerical and geometrical primitives of the postulated language could be detected, both in isolation and within the sequences. These results suggest that the human brain detects sequence regularities at multiple nested levels and uses them to compress long sequences in working memory.
Damiano Azzalini; Anne Buot; Stefano Palminteri; Catherine Tallon-Baudry
Responses to heartbeats in ventromedial prefrontal cortex contribute to subjective preference-based decisions Journal Article
In: Journal of Neuroscience, vol. 41, no. 23, pp. 5102–5114, 2021.
Forrest Gump or The Matrix? Preference-based decisions are subjective and entail self-reflection. However, these self-related features are unaccounted for by known neural mechanisms of valuation and choice. Self-related processes have been linked to a basic interoceptive biological mechanism, the neural monitoring of heartbeats, in particular in ventromedial prefrontal cortex (vmPFC), a region also involved in value encoding. We thus hypothesized a functional coupling between the neural monitoring of heartbeats and the precision of value encoding in vmPFC. Human participants of both sexes were presented with pairs of movie titles. They indicated either which movie they preferred or performed a control objective visual discrimination that did not require self-reflection. Using magnetoencephalography, we measured heartbeat-evoked responses (HERs) before option presentation and confirmed that HERs in vmPFC were larger when preparing for the subjective, self-related task. We retrieved the expected cortical value network during choice with time-resolved statistical modeling. Crucially, we show that larger HERs before option presentation are followed by stronger value encoding during choice in vmPFC. This effect is independent of overall vmPFC baseline activity. The neural interaction between HERs and value encoding predicted preference-based choice consistency over time, accounting for both interindividual differences and trial-to-trial fluctuations within individuals. Neither cardiac activity nor arousal fluctuations could account for any of the effects. HERs did not interact with the encoding of perceptual evidence in the discrimination task. Our results show that the self-reflection underlying preference-based decisions involves HERs, and that HER integration to subjective value encoding in vmPFC contributes to preference stability.
Anne Buot; Damiano Azzalini; Maximilien Chaumon; Catherine Tallon-Baudry
Does stroke volume influence heartbeat evoked responses? Journal Article
In: Biological Psychology, vol. 165, pp. 108165, 2021.
We know surprisingly little on how heartbeat-evoked responses (HERs) vary with cardiac parameters. Here, we measured both stroke volume, or volume of blood ejected at each heartbeat, with impedance cardiography, and HER amplitude with magneto-encephalography, in 21 male and female participants at rest with eyes open. We observed that HER co-fluctuates with stroke volume on a beat-to-beat basis, but only when no correction for cardiac artifact was performed. This highlights the importance of an ICA correction tailored to the cardiac artifact. We also observed that easy-to-measure cardiac parameters (interbeat intervals, ECG amplitude) are sensitive to stroke volume fluctuations and can be used as proxies when stroke volume measurements are not available. Finally, interindividual differences in stroke volume were reflected in MEG data, but whether this effect is locked to heartbeats is unclear. Altogether, our results question assumptions on the link between stroke volume and HERs.
Jonathan Daume; Peng Wang; Alexander Maye; Dan Zhang; Andreas K. Engel
Non-rhythmic temporal prediction involves phase resets of low-frequency delta oscillations Journal Article
In: NeuroImage, vol. 224, pp. 117376, 2021.
The phase of neural oscillatory signals aligns to the predicted onset of upcoming stimulation. Whether such phase alignments represent phase resets of underlying neural oscillations or just rhythmically evoked activity, and whether they can be observed in a rhythm-free visual context, however, remains unclear. Here, we recorded the magnetoencephalogram while participants were engaged in a temporal prediction task, judging the visual or tactile reappearance of a uniformly moving stimulus. The prediction conditions were contrasted with a control condition to dissociate phase adjustments of neural oscillations from stimulus-driven activity. We observed stronger delta band inter-trial phase consistency (ITPC) in a network of sensory, parietal and frontal brain areas, but no power increase reflecting stimulus-driven or prediction-related evoked activity. Delta ITPC further correlated with prediction performance in the cerebellum and visual cortex. Our results provide evidence that phase alignments of low-frequency neural oscillations underlie temporal predictions in a non-rhythmic visual and crossmodal context.
Linda Drijvers; Ole Jensen; Eelke Spaak
Rapid invisible frequency tagging reveals nonlinear integration of auditory and visual information Journal Article
In: Human Brain Mapping, vol. 42, no. 4, pp. 1138–1152, 2021.
During communication in real-life settings, the brain integrates information from auditory and visual modalities to form a unified percept of our environment. In the current magnetoencephalography (MEG) study, we used rapid invisible frequency tagging (RIFT) to generate steady-state evoked fields and investigated the integration of audiovisual information in a semantic context. We presented participants with videos of an actress uttering action verbs (auditory; tagged at 61 Hz) accompanied by a gesture (visual; tagged at 68 Hz, using a projector with a 1,440 Hz refresh rate). Integration difficulty was manipulated by lower-order auditory factors (clear/degraded speech) and higher-order visual factors (congruent/incongruent gesture). We identified MEG spectral peaks at the individual (61/68 Hz) tagging frequencies. We furthermore observed a peak at the intermodulation frequency of the auditory and visually tagged signals (fvisual − fauditory = 7 Hz), specifically when lower-order integration was easiest because signal quality was optimal. This intermodulation peak is a signature of nonlinear audiovisual integration, and was strongest in left inferior frontal gyrus and left temporal regions; areas known to be involved in speech-gesture integration. The enhanced power at the intermodulation frequency thus reflects the ease of lower-order audiovisual integration and demonstrates that speech-gesture information interacts in higher-order language areas. Furthermore, we provide a proof-of-principle of the use of RIFT to study the integration of audiovisual stimuli, in relation to, for instance, semantic context.
Stefan Dürschmid; Andre Maric; Marcel S. Kehl; Robert T Knight; Hermann Hinrichs; Hans-Jochen Heinze
Fronto-temporal regulation of subjective value to suppress impulsivity in intertemporal choices Journal Article
In: Journal of Neuroscience, vol. 41, pp. 1727–1737, 2021.
Impulsive decisions arise from preferring smaller but sooner rewards compared to larger but later rewards. How neural activity and attention to choice alternatives contribute to reward decisions during temporal discounting is not clear. Here we probed (i) attention to and (ii) neural representation of delay and reward information in humans (both sexes) engaged in choices. We studied behavioral and frequency specific dynamics supporting impulsive decisions on a fine-grained temporal scale using eye tracking and magnetoencephalographic (MEG) recordings. In one condition participants had to decide for themselves but pretended to decide for their best friend in a second prosocial condition, which required perspective taking. Hence, conditions varied in the value for themselves versus that pretending to choose for another person. Stronger impulsivity was reliably found across three independent groups for prosocial decisions. Eye tracking revealed a systematic shift of attention from the delay to the reward information and differences in eye tracking between conditions predicted differences in discounting. High frequency activity (HFA: 175-250 Hz) distributed over right fronto-temporal sensors correlated with delay and reward information in consecutive temporal intervals for high value decisions for oneself but not the friend. Collectively the results imply that the HFA recorded over fronto-temporal MEG sensors plays a critical role in choice option integration.
Silvia L. Isabella; J. Allan Cheyne; Douglas Cheyne
Inhibitory control in the absence of awareness: Interactions between frontal and motor cortex oscillations mediate implicitly learned responses Journal Article
In: Frontiers in Human Neuroscience, vol. 15, pp. 786035, 2021.
Cognitive control of action is associated with conscious effort and is hypothesised to be reflected by increased frontal theta activity. However, the functional role of these increases in theta power, and how they contribute to cognitive control remains unknown. We conducted an MEG study to test the hypothesis that frontal theta oscillations interact with sensorimotor signals in order to produce controlled behaviour, and that the strength of these interactions will vary with the amount of control required. We measured neuromagnetic activity in 16 healthy adults performing a response inhibition (Go/Switch) task, known from previous work to modulate cognitive control requirements using hidden patterns of Go and Switch cues. Learning was confirmed by reduced reaction times (RT) to patterned compared to random Switch cues. Concurrent measures of pupil diameter revealed changes in subjective cognitive effort with stimulus probability, even in the absence of measurable behavioural differences, revealing instances of covert variations in cognitive effort. Significant theta oscillations were found in five frontal brain regions, with theta power in the right middle frontal and right premotor cortices parametrically increasing with cognitive effort. Similar increases in oscillatory power were also observed in motor cortical gamma, suggesting an interaction. Right middle frontal and right precentral theta activity predicted changes in pupil diameter across all experimental conditions, demonstrating a close relationship between frontal theta increases and cognitive control. Although no theta-gamma cross-frequency coupling was found, long-range theta phase coherence among the five significant sources between bilateral middle frontal, right inferior frontal, and bilateral premotor areas was found, thus providing a mechanism for the relay of cognitive control between frontal and motor areas via theta signalling. Furthermore, this provides the first evidence for the sensitivity of frontal theta oscillations to implicit motor learning and its effects on cognitive load. More generally these results present a possible a mechanism for this frontal theta network to coordinate response preparation, inhibition and execution.
Hamid Karimi-Rouzbahani; Alexandra Woolgar; Anina N. Rich
Neural signatures of vigilance decrements predict behavioural errors before they occur Journal Article
In: eLife, vol. 10, pp. e60563, 2021.
There are many monitoring environments, such as railway control, in which lapses of attention can have tragic consequences. Problematically, sustained monitoring for rare targets is difficult, with more misses and longer reaction times over time. What changes in the brain underpin these ‘vigilance decrements'? We designed a multiple-object monitoring (MOM) paradigm to examine how the neural representation of information varied with target frequency and time performing the task. Behavioural performance decreased over time for the rare target (monitoring) condition, but not for a frequent target (active) condition. This was mirrored in neural decoding using magnetoencephalography: coding of critical information declined more during monitoring versus active conditions along the experiment. We developed new analyses that can predict behavioural errors from the neural data more than a second before they occurred. This facilitates pre-empting behavioural errors due to lapses in attention and provides new insight into the neural correlates of vigilance decrements.
Anna M. Monk; Daniel N. Barry; Vladimir Litvak; Gareth R. Barnes; Eleanor A. Maguire
Watching movies unfold, a frame-by-frame analysis of the associated neural dynamics Journal Article
In: eNeuro, vol. 8, no. 4, pp. 1–12, 2021.
Our lives unfold as sequences of events. We experience these events as seamless, although they are composed of individual images captured in between the interruptions imposed by eye blinks and saccades. Events typically involve visual imagery from the real world (scenes), and the hippocampus is frequently en-gaged in this context. It is unclear, however, whether the hippocampus would be similarly responsive to unfolding events that involve abstract imagery. Addressing this issue could provide insights into the nature of its contribution to event processing, with relevance for theories of hippocampal function. Consequently, during magnetoencephalography (MEG), we had female and male humans watch highly matched unfolding movie events composed of either scene image frames that reflected the real world, or frames depicting abstract pat-terns. We examined the evoked neuronal responses to each image frame along the time course of the movie events. Only one difference between the two conditions was evident, and that was during the viewing of the first image frame of events, detectable across frontotemporal sensors. Further probing of this difference using source reconstruction revealed greater engagement of a set of brain regions across parietal, frontal, premotor, and cerebellar cortices, with the largest change in broadband (1–30 Hz) power in the hippocampus during scene-based movie events. Hippocampal engagement during the first image frame of scene-based events could reflect its role in registering a recognizable context perhaps based on templates or schemas. The hippo-campus, therefore, may help to set the scene for events very early on.
Anna M. Monk; Marshall A. Dalton; Gareth R. Barnes; Eleanor A. Maguire
The role of hippocampal-ventromedial prefrontal cortex neural dynamics in building mental representations Journal Article
In: Journal of Cognitive Neuroscience, vol. 33, no. 1, pp. 89–103, 2021.
The hippocampus and ventromedial prefrontal cortex (vmPFC) play key roles in numerous cognitive domains including mind-wandering, episodic memory and imagining the future. Perspectives differ on precisely how they support these diverse functions, but there is general agreement that it involves constructing representations comprised of numerous elements. Visual scenes have been deployed extensively in cognitive neuroscience because they are paradigmatic multi-element stimuli. However, it remains unclear whether scenes, rather than other types of multi-feature stimuli, preferentially engage hippocampus and vmPFC. Here we leveraged the high temporal resolution of magnetoencephalography to test participants as they gradually built scene imagery from three successive auditorily-presented object descriptions and an imagined 3D space. This was contrasted with constructing mental images of non-scene arrays that were composed of three objects and an imagined 2D space. The scene and array stimuli were, therefore, highly matched, and this paradigm permitted a closer examination of step-by-step mental construction than has been undertaken previously. We observed modulation of theta power in our two regions of interest -anterior hippocampus during the initial stage, and in vmPFC during the first two stages, of scene relative to array construction. Moreover, the scene-specific anterior hippocampal activity during the first construction stage was driven by the vmPFC, with mutual entrainment between the two brain regions thereafter. These findings suggest that hippocampal and vmPFC neural activity is especially tuned to scene representations during the earliest stage of their formation, with implications for theories of how these brain areas enable cognitive functions such as episodic memory.
Peter R. Murphy; Niklas Wilming; Diana C. Hernandez-Bocanegra; Genis Prat-Ortega; Tobias H. Donner
Adaptive circuit dynamics across human cortex during evidence accumulation in changing environments Journal Article
In: Nature Neuroscience, vol. 24, no. 7, pp. 987–997, 2021.
Many decisions under uncertainty entail the temporal accumulation of evidence that informs about the state of the environment. When environments are subject to hidden changes in their state, maximizing accuracy and reward requires non-linear accumulation of evidence. How this adaptive, non-linear computation is realized in the brain is unknown. We analyzed human behavior and cortical population activity (measured with magnetoencephalography) recorded during visual evidence accumulation in a changing environment. Behavior and decision-related activity in cortical regions involved in action planning exhibited hallmarks of adaptive evidence accumulation, which could also be implemented by a recurrent cortical microcircuit. Decision dynamics in action-encoding parietal and frontal regions were mirrored in a frequency-specific modulation of the state of the visual cortex that depended on pupil-linked arousal and the expected probability of change. These findings link normative decision computations to recurrent cortical circuit dynamics and highlight the adaptive nature of decision-related feedback to the sensory cortex.
J. A. Nij Bijvank; E. M. M. Strijbis; I. M. Nauta; S. D. Kulik; L. J. Balk; C. J. Stam; A. Hillebrand; J. J. G. Geurts; B. M. J. Uitdehaag; L. J. Rijn; A. Petzold; M. M. Schoonheim
Impaired saccadic eye movements in multiple sclerosis are related to altered functional connectivity of the oculomotor brain network Journal Article
In: NeuroImage: Clinical, vol. 32, pp. 102848, 2021.
Background: Impaired eye movements in multiple sclerosis (MS) are common and could represent a non-invasive and accurate measure of (dys)functioning of interconnected areas within the complex brain network. The aim of this study was to test whether altered saccadic eye movements are related to changes in functional connectivity (FC) in patients with MS. Methods: Cross-sectional eye movement (pro-saccades and anti-saccades) and magnetoencephalography (MEG) data from the Amsterdam MS cohort were included from 176 MS patients and 33 healthy controls. FC was calculated between all regions of the Brainnetome atlas in six conventional frequency bands. Cognitive function and disability were evaluated by previously validated measures. The relationships between saccadic parameters and both FC and clinical scores in MS patients were analysed using multivariate linear regression models. Results: In MS pro- and anti-saccades were abnormal compared to healthy controls A relationship of saccadic eye movements was found with FC of the oculomotor network, which was stronger for regional than global FC. In general, abnormal eye movements were related to higher delta and theta FC but lower beta FC. Strongest associations were found for pro-saccadic latency and FC of the precuneus (beta band $beta$ = -0.23
Anastasia O. Ovchinnikova; Anatoly N. Vasilyev; Ivan P. Zubarev; Bogdan L. Kozyrskiy; Sergei L. Shishkin
MEG-based detection of voluntary eye fixations used to control a computer Journal Article
In: Frontiers in Neuroscience, vol. 15, pp. 619591, 2021.
Gaze-based input is an efficient way of hand-free human-computer interaction. However, it suffers from the inability of gaze-based interfaces to discriminate voluntary and spontaneous gaze behaviors, which are overtly similar. Here, we demonstrate that voluntary eye fixations can be discriminated from spontaneous ones using short segments of magnetoencephalography (MEG) data measured immediately after the fixation onset. Recently proposed convolutional neural networks (CNNs), linear finite impulse response filters CNN (LF-CNN) and vector autoregressive CNN (VAR-CNN), were applied for binary classification of the MEG signals related to spontaneous and voluntary eye fixations collected in healthy participants (n = 25) who performed a game-like task by fixating on targets voluntarily for 500 ms or longer. Voluntary fixations were identified as those followed by a fixation in a special confirmatory area. Spontaneous vs. voluntary fixation-related single-trial 700 ms MEG segments were non-randomly classified in the majority of participants, with the group average cross-validated ROC AUC of 0.66 ± 0.07 for LF-CNN and 0.67 ± 0.07 for VAR-CNN (M ± SD). When the time interval, from which the MEG data were taken, was extended beyond the onset of the visual feedback, the group average classification performance increased up to 0.91. Analysis of spatial patterns contributing to classification did not reveal signs of significant eye movement impact on the classification results. We conclude that the classification of MEG signals has a certain potential to support gaze-based interfaces by avoiding false responses to spontaneous eye fixations on a single-trial basis. Current results for intention detection prior to gaze-based interface's feedback, however, are not sufficient for online single-trial eye fixation classification using MEG data alone, and further work is needed to find out if it could be used in practical applications.
Yali Pan; Steven Frisson; Ole Jensen
Neural evidence for lexical parafoveal processing Journal Article
In: Nature Communications, vol. 12, pp. 5234, 2021.
In spite of the reduced visual acuity, parafoveal information plays an important role in natural reading. However, competing models on reading disagree on whether words are previewed parafoveally at the lexical level. We find neural evidence for lexical parafoveal processing by combining a rapid invisible frequency tagging (RIFT) approach with magnetoencephalography (MEG) and eye-tracking. In a silent reading task, target words are tagged (flickered) subliminally at 60 Hz. The tagging responses measured when fixating on the pre-target word reflect parafoveal processing of the target word. We observe stronger tagging responses during pre-target fixations when followed by low compared with high lexical frequency targets. Moreover, this lexical parafoveal processing is associated with individual reading speed. Our findings suggest that reading unfolds in the fovea and parafovea simultaneously to support fluent reading.
Thomas Pfeffer; Adrian Ponce-Alvarez; Konstantinos Tsetsos; Thomas Meindertsma; Christoffer Julius Gahnström; Ruud Lucas Brink; Guido Nolte; Andreas Karl Engel; Gustavo Deco; Tobias Hinrich Donner
Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability Journal Article
In: Science Advances, vol. 7, no. 29, pp. eabf5620, 2021.
Influential theories postulate distinct roles of catecholamines and acetylcholine in cognition and behavior. However, previous physiological work reported similar effects of these neuromodulators on the response properties (specifically, the gain) of individual cortical neurons. Here, we show a double dissociation between the effects of catecholamines and acetylcholine at the level of large-scale interactions between cortical areas in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. An acetylcholine boost decreased interactions during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: The local excitation-inhibition balance (more strongly increased by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted noisier decision-making, which we confirmed for both perceptual and value-based choice behavior. Our work highlights specific circuit mechanisms for shaping cortical network interactions and behavioral variability by key neuromodulatory systems.
Ella Podvalny; Leana E. King; Biyu J. He
Spectral signature and behavioral consequence of spontaneous shifts of pupil-linked arousal in human Journal Article
In: eLife, vol. 10, pp. e68265, 2021.
Arousal levels perpetually rise and fall spontaneously. How markers of arousal—pupil size and frequency content of brain activity—relate to each other and influence behavior in humans is poorly understood. We simultaneously monitored magnetoencephalography and pupil in healthy volunteers at rest and during a visual perceptual decision-making task. Spontaneously varying pupil size correlates with power of brain activity in most frequency bands across large-scale resting-state cortical networks. Pupil size recorded at prestimulus baseline correlates with subsequent shifts in detection bias (c) and sensitivity (d'). When dissociated from pupil-linked state, prestimulus spectral power of resting state networks still predicts perceptual behavior. Fast spontaneous pupil constriction and dilation correlate with large-scale brain activity as well but not perceptual behavior. Our results illuminate the relation between central and peripheral arousal markers and their respective roles in human perceptual decision-making.
Isabelle A. Rosenthal; Shridhar R. Singh; Katherine L. Hermann; Dimitrios Pantazis; Bevil R. Conway
Color space geometry uncovered with magnetoencephalography Journal Article
In: Current Biology, vol. 31, no. 3, pp. 515–526, 2021.
The geometry that describes the relationship among colors, and the neural mechanisms that support color vision, are unsettled. Here, we use multivariate analyses of measurements of brain activity obtained with magnetoencephalography to reverse-engineer a geometry of the neural representation of color space. The analyses depend upon determining similarity relationships among the spatial patterns of neural responses to different colors and assessing how these relationships change in time. We evaluate the approach by relating the results to universal patterns in color naming. Two prominent patterns of color naming could be accounted for by the decoding results: the greater precision in naming warm colors compared to cool colors evident by an interaction of hue and lightness, and the preeminence among colors of reddish hues. Additional experiments showed that classifiers trained on responses to color words could decode color from data obtained using colored stimuli, but only at relatively long delays after stimulus onset. These results provide evidence that perceptual representations can give rise to semantic representations, but not the reverse. Taken together, the results uncover a dynamic geometry that provides neural correlates for color appearance and generates new hypotheses about the structure of color space.
Rodolfo Solís-Vivanco; Ole Jensen; Mathilde Bonnefond
New insights on the ventral attention network: Active suppression and involuntary recruitment during a bimodal task Journal Article
In: Human Brain Mapping, vol. 42, no. 6, pp. 1699–1713, 2021.
Detection of unexpected, yet relevant events is essential in daily life. fMRI studies have revealed the involvement of the ventral attention network (VAN), including the temporo-parietal junction (TPJ), in such process. In this MEG study with 34 participants (17 women), we used a bimodal (visual/auditory) attention task to determine the neuronal dynamics associated with suppression of the activity of the VAN during top-down attention and its recruitment when information from the unattended sensory modality is involuntarily integrated. We observed an anticipatory power increase of alpha/beta oscillations (12–20 Hz, previously associated with functional inhibition) in the VAN following a cue indicating the modality to attend. Stronger VAN power increases were associated with better task performance, suggesting that the VAN suppression prevents shifting attention to distractors. Moreover, the TPJ was synchronized with the frontal eye field in that frequency band, indicating that the dorsal attention network (DAN) might participate in such suppression. Furthermore, we found a 12–20 Hz power decrease and enhanced synchronization, in both the VAN and DAN, when information between sensory modalities was congruent, suggesting an involvement of these networks when attention is involuntarily enhanced due to multisensory integration. Our results show that effective multimodal attentional allocation includes the modulation of the VAN and DAN through upper-alpha/beta oscillations. Altogether these results indicate that the suppressing role of alpha/beta oscillations might operate beyond sensory regions.
Aurélien Weiss; Valérian Chambon; Junseok K. Lee; Jan Drugowitsch; Valentin Wyart
Interacting with volatile environments stabilizes hidden-state inference and its brain signatures Journal Article
In: Nature Communications, vol. 12, pp. 2228, 2021.
Making accurate decisions in uncertain environments requires identifying the generative cause of sensory cues, but also the expected outcomes of possible actions. Although both cognitive processes can be formalized as Bayesian inference, they are commonly studied using different experimental frameworks, making their formal comparison difficult. Here, by framing a reversal learning task either as cue-based or outcome-based inference, we found that humans perceive the same volatile environment as more stable when inferring its hidden state by interaction with uncertain outcomes than by observation of equally uncertain cues. Multivariate patterns of magnetoencephalographic (MEG) activity reflected this behavioral difference in the neural interaction between inferred beliefs and incoming evidence, an effect originating from associative regions in the temporal lobe. Together, these findings indicate that the degree of control over the sampling of volatile environments shapes human learning and decision-making under uncertainty.
Benjamin J. Stauch; Alina Peter; Heike Schuler; Pascal Fries
Stimulus-specific plasticity in human visual gamma-band activity and functional connectivity Journal Article
In: eLife, vol. 10, pp. e68240, 2021.
Under natural conditions, the visual system often sees a given input repeatedly. This provides an opportunity to optimize processing of the repeated stimuli. Stimulus repetition has been shown to strongly modulate neuronal-gamma band synchronization, yet crucial questions remained open. Here we used magnetoencephalography in 30 human subjects and find that gamma decreases across ≈10 repetitions and then increases across further repetitions, revealing plastic changes of the activated neuronal circuits. Crucially, increases induced by one stimulus did not affect responses to other stimuli, demonstrating stimulus specificity. Changes partially persisted when the inducing stimulus was repeated after 25 minutes of intervening stimuli. They were strongest in early visual cortex and increased interareal feedforward influences. Our results suggest that early visual cortex gamma synchronization enables adaptive neuronal processing of recurring stimuli. These and previously reported changes might be due to an interaction of oscillatory dynamics with established synaptic plasticity mechanisms.
Yu Takagi; Laurence Tudor Hunt; Mark W. Woolrich; Timothy E. J. Behrens; Miriam C. Klein-Flügge
Adapting non-invasive human recordings along multiple task-axes shows unfolding of spontaneous and over-trained choice Journal Article
In: eLife, vol. 10, pp. 1–27, 2021.
Choices rely on a transformation of sensory inputs into motor responses. Using invasive single neuron recordings, the evolution of a choice process has been tracked by projecting population neural responses into state spaces. Here, we develop an approach that allows us to recover similar trajectories on a millisecond timescale in non-invasive human recordings. We selectively suppress activity related to three task-axes, relevant and irrelevant sensory inputs and response direction, in magnetoencephalography data acquired during context-dependent choices. Recordings from premotor cortex show a progression from processing sensory input to processing the response. In contrast to previous macaque recordings, information related to choice-irrelevant features is represented more weakly than choice-relevant sensory information. To test whether this mechanistic difference between species is caused by extensive over-training common in non-human primate studies, we trained humans on >20,000 trials of the task. Choice-irrelevant features were still weaker than relevant features in premotor cortex after over-training.
Elisa Infanti; D. Samuel Schwarzkopf
Mapping sequences can bias population receptive field estimates Journal Article
In: NeuroImage, vol. 211, pp. 116636, 2020.
Population receptive field (pRF) modelling is a common technique for estimating the stimulus-selectivity of populations of neurons using neuroimaging. Here, we aimed to address if pRF properties estimated with this method depend on the spatio-temporal structure and the predictability of the mapping stimulus. We mapped the polar angle preference and tuning width of voxels in visual cortex (V1–V4) of healthy, adult volunteers. We compared sequences sweeping orderly through the visual field or jumping from location to location employing stimuli of different width (45° vs 6°) and cycles of variable duration (8s vs 60s). While we did not observe any systematic influence of stimulus predictability, the temporal structure of the sequences significantly affected tuning width estimates. Ordered designs with large wedges and short cycles produced systematically smaller estimates than random sequences. Interestingly, when we used small wedges and long cycles, we obtained larger tuning width estimates for ordered than random sequences. We suggest that ordered and random mapping protocols show different susceptibility to other design choices such as stimulus type and duration of the mapping cycle and can produce significantly different pRF results.
Andrea Grant; Gregory J. Metzger; Pierre François Van de Moortele; Gregor Adriany; Cheryl Olman; Lin Zhang; Joseph Koopermeiners; Yiğitcan Eryaman; Margaret Koeritzer; Meredith E. Adams; Thomas R. Henry; Kamil Uğurbil
10.5 T MRI static field effects on human cognitive, vestibular, and physiological function Journal Article
In: Magnetic Resonance Imaging, vol. 73, pp. 163–176, 2020.
Purpose: To perform a pilot study to quantitatively assess cognitive, vestibular, and physiological function during and after exposure to a magnetic resonance imaging (MRI) system with a static field strength of 10.5 Tesla at multiple time scales. Methods: A total of 29 subjects were exposed to a 10.5 T MRI field and underwent vestibular, cognitive, and physiological testing before, during, and after exposure; for 26 subjects, testing and exposure were repeated within 2–4 weeks of the first visit. Subjects also reported sensory perceptions after each exposure. Comparisons were made between short and long term time points in the study with respect to the parameters measured in the study; short term comparison included pre-vs-isocenter and pre-vs-post (1–24 h), while long term compared pre-exposures 2–4 weeks apart. Results: Of the 79 comparisons, 73 parameters were unchanged or had small improvements after magnet exposure. The exceptions to this included lower scores on short term (i.e. same day) executive function testing, greater isocenter spontaneous eye movement during visit 1 (relative to pre-exposure), increased number of abnormalities on videonystagmography visit 2 versus visit 1 and a mix of small increases (short term visit 2) and decreases (short term visit 1) in blood pressure. In addition, more subjects reported metallic taste at 10.5 T in comparison to similar data obtained in previous studies at 7 T and 9.4 T. Conclusion: Initial results of 10.5 T static field exposure indicate that 1) cognitive performance is not compromised at isocenter, 2) subjects experience increased eye movement at isocenter, and 3) subjects experience small changes in vital signs but no field-induced increase in blood pressure. While small but significant differences were found in some comparisons, none were identified as compromising subject safety. A modified testing protocol informed by these results was devised with the goal of permitting increased enrollment while providing continued monitoring to evaluate field effects.
Joseph C. Griffis; Nicholas V. Metcalf; Maurizio Corbetta; Gordon L. Shulman
Damage to the shortest structural paths between brain regions is associated with disruptions of resting-state functional connectivity after stroke Journal Article
In: NeuroImage, vol. 210, pp. 116589, 2020.
Focal brain lesions disrupt resting-state functional connectivity, but the underlying structural mechanisms are unclear. Here, we examined the direct and indirect effects of structural disconnections on resting-state functional connectivity in a large sample of sub-acute stroke patients with heterogeneous brain lesions. We estimated the impact of each patient's lesion on the structural connectome by embedding the lesion in a diffusion MRI streamline tractography atlas constructed using data from healthy individuals. We defined direct disconnections as the loss of direct structural connections between two regions, and indirect disconnections as increases in the shortest structural path length between two regions that lack direct structural connections. We then tested the hypothesis that functional connectivity disruptions would be more severe for disconnected regions than for regions with spared connections. On average, nearly 20% of all region pairs were estimated to be either directly or indirectly disconnected by the lesions in our sample, and extensive disconnections were associated primarily with damage to deep white matter locations. Importantly, both directly and indirectly disconnected region pairs showed more severe functional connectivity disruptions than region pairs with spared direct and indirect connections, respectively, although functional connectivity disruptions tended to be most severe between region pairs that sustained direct structural disconnections. Together, these results emphasize the widespread impacts of focal brain lesions on the structural connectome and show that these impacts are reflected by disruptions of the functional connectome. Further, they indicate that in addition to direct structural disconnections, lesion-induced increases in the structural shortest path lengths between indirectly structurally connected region pairs provide information about the remote functional disruptions caused by focal brain lesions.
Marcus Grueschow; Birgit Kleim; Christian C. Ruff
Role of the locus coeruleus arousal system in cognitive control Journal Article
In: Journal of Neuroendocrinology, vol. 32, pp. 1–11, 2020.
Cognitive control lies at the core of human adaptive behaviour. Humans vary substantially in their ability to execute cognitive control with respect to optimally facing environmental challenges, although the neural origins of this heterogeneity are currently not well understood. Recent theoretical frameworks implicate the locus coeruleus noradrenergic arousal system (LC-NE) in that process. Invasive neurophysiological work in rodents has shown that the LC-NE is an important homeostatic control centre of the body. LC-NE innervates the entire neocortex and has particularly strong connections with the cingulate gyrus. In the present study, using a response conflict task, functional magnetic resonance imaging and concurrent pupil dilation measures (a proxy for LC-NE firing), we provide empirical evidence for a decisive role of the LC-NE in cognitive control in humans. We show that the level of individual behavioural adjustment in cognitive control relates to the level of functional coupling between LC-NE and the dorsomedial prefrontal cortex, as well as dorsolateral prefrontal cortex. Moreover, we show that the pupil is substantially more dilated during conflict trials requiring behavioural adjustment than during no conflict trials. In addition, we explore a potential relationship between pupil dilation and neural activity during choice conflict adjustments. Our data provide novel insight into arousal-related influences on cognitive control and suggest pupil dilation as a potential external marker for endogenous neural processes involved in optimising behavioural control. Our results may also be clinically relevant for a variety of pathologies where cognitive control is compromised, such as anxiety, depression, addiction and post-traumatic stress disorder.
Arvid Guterstam; Branden J. Bio; Andrew I. Wilterson; Michael S. A. Graziano
Temporo-parietal cortex involved in modeling one's own and others' attention Journal Article
In: eLife, vol. 10, pp. e63551, 2020.
In a traditional view, in social cognition, attention is equated with gaze and people track attention by tracking other people's gaze. Here we used fMRI to test whether the brain represents attention in a richer manner. People read stories describing an agent (either oneself or someone else) directing attention to an object in one of two ways: either internally directed (endogenous) or externally induced (exogenous). We used multivoxel pattern analysis to examine how brain areas within the theory-of-mind network encoded attention type and agent type. Brain activity patterns in the left temporo-parietal junction (TPJ) showed significant decoding of information about endogenous versus exogenous attention. The left TPJ, left superior temporal sulcus (STS), precuneus, and medial prefrontal cortex (MPFC) significantly decoded agent type (self versus other). These findings show that the brain constructs a rich model of one's own and others' attentional state, possibly aiding theory of mind.
Arvid Guterstam; Andrew I. Wilterson; Davis Wachtell; Michael S. A. Graziano
Other people's gaze encoded as implied motion in the human brain Journal Article
In: Proceedings of the National Academy of Sciences, vol. 117, no. 23, pp. 13162–13167, 2020.
Keeping track of other people's gaze is an essential task in social cognition and key for successfully reading other people's intentions and beliefs (theory of mind). Recent behavioral evidence suggests that we construct an implicit model of other people's gaze, which may incorporate physically incoherent attributes such as a construct of force-carrying beams that emanate from the eyes. Here, we used functional magnetic resonance imaging and multivoxel pattern analysis to test the prediction that the brain encodes gaze as implied motion streaming from an agent toward a gazed-upon object. We found that a classifier, trained to discriminate the direction of visual motion, significantly decoded the gaze direction in static images depicting a sighted face, but not a blindfolded one, from brain activity patterns in the human motion-sensitive middle temporal complex (MT+) and temporo-parietal junction (TPJ). Our results demonstrate a link between the visual motion system and social brain mechanisms, in which the TPJ, a key node in theory of mind, works in concert with MT+ to encode gaze as implied motion. This model may be a fundamental aspect of social cognition that allows us to efficiently connect agents with the objects of their attention. It is as if the brain draws a quick visual sketch with moving arrows to help keep track of who is attending to what. This implicit, fluid-flow model of other people's gaze may help explain culturally universal myths about the mind as an energy-like, flowing essence.
Kristen R. Hamilton; Jason F. Smith; Stefanie F. Gonçalves; Jazlyn A. Nketia; Olivia N. Tasheuras; Mark Yoon; Katya Rubia; Theresa J. Chirles; Carl W. Lejuez; Alexander J. Shackman
Striatal bases of temporal discounting in early adolescents Journal Article
In: Neuropsychologia, vol. 144, pp. 107492, 2020.
Steeper rates of temporal discounting—the degree to which smaller-sooner (SS) rewards are preferred over larger-later (LL) ones—have been associated with impulsive and ill-advised behaviors in adolescence. Yet, the underlying neural systems remain poorly understood. Here we used a well-established temporal discounting paradigm and functional MRI (fMRI) to examine engagement of the striatum—including the caudate, putamen, and ventral striatum (VS)—in early adolescence (13–15 years; N = 27). Analyses provided evidence of enhanced activity in the caudate and VS during impulsive choice. Exploratory analyses revealed that trait impulsivity was associated with heightened putamen activity during impulsive choices. A more nuanced pattern was evident in the cortex, with the dorsolateral prefrontal cortex mirroring the putamen and posterior parietal cortex showing the reverse association. Taken together, these observations provide an important first glimpse at the distributed neural systems underlying economic choice and trait-like individual differences in impulsivity in the early years of adolescence, setting the stage for prospective-longitudinal and intervention research.
Christoph Helmchen; Björn Machner; Matthias Rother; Peer Spliethoff; Martin Göttlich; Andreas Sprenger
Effects of galvanic vestibular stimulation on resting state brain activity in patients with bilateral vestibulopathy Journal Article
In: Human Brain Mapping, vol. 41, no. 9, pp. 2527–2547, 2020.
We examined the effect of galvanic vestibular stimulation (GVS) on resting state brain activity using fMRI (rs-fMRI) in patients with bilateral vestibulopathy. Based on our previous findings, we hypothesized that GVS, which excites the vestibular nerve fibers, (a) increases functional connectivity in temporoparietal regions processing vestibular signals, and (b) alleviates abnormal visual–vestibular interaction. Rs-fMRI of 26 patients and 26 age-matched healthy control subjects was compared before and after GVS. The stimulation elicited a motion percept in all participants. Using different analyses (degree centrality, DC; fractional amplitude of low frequency fluctuations [fALFF] and seed-based functional connectivity, FC), group comparisons revealed smaller rs-fMRI in the right Rolandic operculum of patients. After GVS, rs-fMRI increased in the right Rolandic operculum in both groups and in the patients' cerebellar Crus 1 which was related to vestibular hypofunction. GVS elicited a fALFF increase in the visual cortex of patients that was inversely correlated with the patients' rating of perceived dizziness. After GVS, FC between parietoinsular cortex and higher visual areas increased in healthy controls but not in patients. In conclusion, short-term GVS is able to modulate rs-fMRI in healthy controls and BV patients. GVS elicits an increase of the reduced rs-fMRI in the patients' right Rolandic operculum, which may be an important contribution to restore the disturbed visual–vestibular interaction. The GVS-induced changes in the cerebellum and the visual cortex were associated with lower dizziness-related handicaps in patients, possibly reflecting beneficial neural plasticity that might subserve visual–vestibular compensation of deficient self-motion perception.
Lara Henco; Marie Luise Brandi; Juha M. Lahnakoski; Andreea O. Diaconescu; Christoph Mathys; Leonhard Schilbach
Bayesian modelling captures inter-individual differences in social belief computations in the putamen and insula Journal Article
In: Cortex, vol. 131, pp. 221–236, 2020.
Computational models of social learning and decision-making provide mechanistic tools to investigate the neural mechanisms that are involved in understanding other people. While most studies employ explicit instructions to learn from social cues, everyday life is characterized by the spontaneous use of such signals (e.g., the gaze of others) to infer on internal states such as intentions. To investigate the neural mechanisms of the impact of gaze cues on learning and decision-making, we acquired behavioural and fMRI data from 50 participants performing a probabilistic task, in which cards with varying winning probabilities had to be chosen. In addition, the task included a computer-generated face that gazed towards one of these cards providing implicit advice. Participants' individual belief trajectories were inferred using a hierarchical Gaussian filter (HGF) and used as predictors in a linear model of neuronal activation. During learning, social prediction errors were correlated with activity in inferior frontal gyrus and insula. During decision-making, the belief about the accuracy of the social cue was correlated with activity in inferior temporal gyrus, putamen and pallidum while the putamen and insula showed activity as a function of individual differences in weighting the social cue during decision-making. Our findings demonstrate that model-based fMRI can give insight into the behavioural and neural aspects of spontaneous social cue integration in learning and decision-making. They provide evidence for a mechanistic involvement of specific components of the basal ganglia in subserving these processes.
John M. Henderson; Jessica E. Goold; Wonil Choi; Taylor R. Hayes
Neural correlates of fixated low-and high-level scene properties during active scene viewing Journal Article
In: Journal of Cognitive Neuroscience, vol. 32, no. 10, pp. 2013–2023, 2020.
During real-world scene perception, viewers actively direct their attention through a scene in a controlled sequence of eye fixations. During each fixation, local scene properties are attended, analyzed, and interpreted. What is the relationship between fixated scene properties and neural activity in the visual cortex? Participants inspected photographs of real-world scenes in an MRI scanner while their eye movements were recorded. Fixation-related fMRI was used tomeasure activation as a function of lower- and higher-level scene properties at fixation, operationalized as edge density and meaning maps, respectively. We found that edge density at fixation was most associated with activation in early visual areas, whereas semantic content at fixation was most associated with activation along the ventral visual streamincluding core object and scene-selective areas (lateral occipital complex, parahippocampal place area, occipital place area, and retrosplenial cortex). The observed activation from semantic content was not accounted for by differences in edge density. The results are consistent with active vision models in which fixation gates detailed visual analysis for fixated scene regions, and this gating influences both lower and higher levels of scene analysis.
Yaseen A. Jamal; Daniel D. Dilks
Rapid topographic reorganization in adult human primary visual cortex (V1) during noninvasive and reversible deprivation Journal Article
In: Proceedings of the National Academy of Sciences, vol. 117, no. 20, pp. 11059–11067, 2020.
Can the primary visual cortex (V1), once wired up in development, change in adulthood? Although numerous studies have demonstrated topographic reorganization in adult V1 following the loss of bottom-up input, others have challenged such findings, offering alternative explanations. Here we use a noninvasive and reversible deprivation paradigm and converging neural and behavioral approaches to address these alternatives in the experimental test case of short-term topographic reorganization in adult human V1. Specifically, we patched one eye in typical adults, thereby depriving the cortical representation of the other eye's blind spot (BS), and immediately tested for topographic reorganization using functional magnetic resonance imaging and psychophysics. Strikingly, within just minutes of eye-patching, the BS representation in V1 began responding to stimuli presented outside of the BS, and these same stimuli were perceived as elongated toward the BS. Thus, we provide converging neural and behavioral evidence of rapid topographic reorganization in adult human V1, and the strongest evidence yet that visual deprivation produces bona fide cortical change.
Andy Jeesu Kim; Brian A. Anderson
Arousal-biased competition explains reduced distraction by reward cues under threat Journal Article
In: eNeuro, vol. 7, no. 4, pp. 1–12, 2020.
Anxiety is an adaptive neural state that promotes rapid responses under heightened vigilance when survival is threatened. Anxiety has consistently been found to potentiate the attentional processing of physically salient stimuli. However, a recent study demonstrated that a threat manipulation reduces attentional capture by reward-associated stimuli, suggesting a more complex relationship between anxiety and the control of attention. The mechanisms by which threat can reduce the distracting quality of stimuli are unknown. In this study, using functional magnetic resonance imaging (fMRI) on human subjects, we examined the neural correlates of attention to previously reward-associated stimuli with and without the threat of unpredictable electric shock. We replicate enhanced distractor-evoked activity throughout the value-driven attention network (VDAN) in addition to enhanced stimulus-evoked activity generally under threat. Importantly, these two factors interacted such that the representation of previously reward-associated distractors was particularly pronounced under threat. Our results from neuroimaging fit well with the principle of arousal-biased competition (ABC), although such effects are typically associated with behavioral measures of increased attention to stimuli that already possess elevated attentional priority. The findings of our study suggest that ABC can be leveraged to support more efficient ignoring of reward cues, revealing new insights into the functional significance of ABC as a mechanism of attentional control, and provide a mechanistic explanation of how threat reduces attention to irrelevant reward information.
Andy Jeesu Kim; Brian A. Anderson
Neural correlates of attentional capture by stimuli previously associated with social reward Journal Article
In: Cognitive Neuroscience, vol. 11, no. 1-2, pp. 5–15, 2020.
Our attention is strongly influenced by reward learning. Stimuli previously associated with monetary reward have been shown to automatically capture attention in both behavioral and neurophysiological studies. Stimuli previously associated with positive social feedback similarly capture attention; however, it is unknown whether such social facilitation of attention relies on similar or dissociable neural systems. Here, we used the value-driven attentional capture paradigm in an fMRI study to identify the neural correlates of attention to stimuli previously associated with social reward. The results reveal learning-dependent priority signals in the contralateral visual cortex, posterior parietal cortex, and caudate tail, similar to studies using monetary reward. An additional priority signal was consistently evident in the right middle frontal gyrus (MFG). Our findings support the notion of a common neural mechanism for directing attention on the basis of selection history that generalizes across different types of reward.
Tamar Kolodny; Michael Paul Schallmo; Jennifer Gerdts; Raphael A. Bernier; Scott O. Murray
Response dissociation in hierarchical cortical circuits: A unique feature of autism spectrum disorder Journal Article
In: Journal of Neuroscience, vol. 40, no. 10, pp. 2269–2281, 2020.
A prominent hypothesis regarding the pathophysiology of autism is that an increase in the balance between neural excitation and inhibition results in an increase in neural responses. However, previous reports of population-level response magnitude in individuals with autism have been inconsistent. Critically, network interactions have not been considered in previous neuroimaging studies of excitation and inhibition imbalance in autism. In particular, a defining characteristic of cortical organization is its hierarchical and interactive structure; sensory and cognitive systems are comprised of networks where later stages inherit and build upon the processing of earlier input stages, and also influence and shape earlier stages by top-down modulation. Here we used the well established connections of the human visual system to examine response magnitudes in a higher-order motion processing region [middle temporal area (MT+)] and its primary input region (V1). Simple visual stimuli were presented to adult individuals with autism spectrum disorders (ASD; n = 24, mean age 23 years, 8 females) and neurotypical controls (n = 24, mean age 22, 8 females) during fMRI scanning. We discovered a strong dissociation of fMRI response magnitude between region MT+ and V1 in individuals with ASD: individuals with high MT+ responses had attenuated V1 responses. The magnitude of MT+ amplification and of V1 attenuation was associated with autism severity, appeared to result from amplified suppressive feedback from MT+ to V1, and was not present in neurotypical controls. Our results reveal the potential role of altered hierarchical network interactions in the pathophysiology of ASD.
Elizabeth S. Lorenc; Annelinde R. E. Vandenbroucke; Derek E. Nee; Floris P. Lange; Mark D'Esposito
Dissociable neural mechanisms underlie currently-relevant, future-relevant, and discarded working memory representations Journal Article
In: Scientific Reports, vol. 10, pp. 11195, 2020.
In daily life, we use visual working memory (WM) to guide our actions. While attending to currently-relevant information, we must simultaneously maintain future-relevant information, and discard information that is no longer relevant. However, the neural mechanisms by which unattended, but future-relevant, information is maintained in working memory, and future-irrelevant information is discarded, are not well understood. Here, we investigated representations of these different information types, using functional magnetic resonance imaging in combination with multivoxel pattern analysis and computational modeling based on inverted encoding model simulations. We found that currently-relevant WM information in the focus of attention was maintained through representations in visual, parietal and posterior frontal brain regions,whereas deliberate forgetting led to suppression of the discarded representations in early visual cortex. In contrast, future-relevant information was neither inhibited nor actively maintained in these areas. These findings suggest that different neural mechanisms underlie the WM representation of currently- and future-relevant information, as compared to information that is discarded from WM.
Simona Monaco; Giulia Malfatti; Jody C. Culham; Luigi Cattaneo; Luca Turella
Decoding motor imagery and action planning in the early visual cortex: Overlapping but distinct neural mechanisms Journal Article
In: NeuroImage, vol. 218, pp. 116981, 2020.
Recent evidence points to a role of the primary visual cortex that goes beyond visual processing into high-level cognitive and motor-related functions, including action planning, even in absence of feedforward visual information. It has been proposed that, at the neural level, motor imagery is a simulation based on motor representations, and neuroimaging studies have shown overlapping and shared activity patterns for motor imagery and action execution in frontal and parietal cortices. Yet, the role of the early visual cortex in motor imagery remains unclear. Here we used multivoxel pattern analyses on functional magnetic resonance imaging (fMRI) data to examine whether the content of motor imagery and action intention can be reliably decoded from the activity patterns in the retinotopic location of the target object in the early visual cortex. Further, we investigated whether the discrimination between specific actions generalizes across imagined and intended movements. Eighteen right-handed human participants (11 females) imagined or performed delayed hand actions towards a centrally located object composed of a small shape attached on a large shape. Actions consisted of grasping the large or small shape, and reaching to the center of the object. We found that despite comparable fMRI signal amplitude for different planned and imagined movements, activity patterns in the early visual cortex, as well as dorsal premotor and anterior intraparietal cortex, accurately represented action plans and action imagery. However, movement content is similar irrespective of whether actions are actively planned or covertly imagined in parietal but not early visual or premotor cortex, suggesting a generalized motor representation only in regions that are highly specialized in object directed grasping actions and movement goals. In sum, action planning and imagery have overlapping but non identical neural mechanisms in the cortical action network.
Cristian Morales; Suril Gohel; Xiaobo Li; Mitchell Scheiman; Bharat B. Biswal; Elio M. Santos; Chang Yaramothu; Tara L. Alvarez
Test–retest reliability of functional magnetic resonance imaging activation for a vergence eye movement task Journal Article
In: Neuroscience Bulletin, vol. 36, no. 5, pp. 506–518, 2020.
Vergence eye movements are the inward and outward rotation of the eyes responsible for binocular coordination. While studies have mapped and investigated the neural substrates of vergence, it is not well understood whether vergence eye movements evoke the blood oxygen level-dependent signal reliably in separate experimental visits. The test–retest reliability of stimulus-induced vergence eye movement tasks during a functional magnetic resonance imaging (fMRI) experiment is important for future randomized clinical trials (RCTs). In this study, we established region of interest (ROI) masks for the vergence neural circuit. Twenty-seven binocularly normal young adults participated in two functional imaging sessions measured on different days on the same 3T Siemens scanner. The fMRI experiments used a block design of sustained visual fixation and rest blocks interleaved between task blocks that stimulated eight or four vergence eye movements. The test–retest reliability of task-activation was assessed using the intraclass correlation coefficient (ICC), and that of spatial extent was assessed using the Dice coefficient. Functional activation during the vergence eye movement task of eight movements compared to rest was repeatable within the primary visual cortex (ICC = 0.8), parietal eye fields (ICC = 0.6), supplementary eye field (ICC = 0.5), frontal eye fields (ICC = 0.5), and oculomotor vermis (ICC = 0.6). The results demonstrate significant test–retest reliability in the ROIs of the vergence neural substrates for functional activation magnitude and spatial extent using the stimulus protocol of a task block stimulating eight vergence eye movements compared to sustained fixation. These ROIs can be used in future longitudinal RCTs to study patient populations with vergence dysfunctions.
Cristian Morales; Suril Gohel; Mitchell Scheiman; Xiaobo Li; Elio M. Santos; Ayushi Sangoi; Tara L. Alvarez
Test-retest of a phoria adaptation stimulus-induced functional MRI experiment Journal Article
In: Journal of Vision, vol. 20, no. 8, pp. 1–15, 2020.
This study was designed to identify the neural substrates activated during a phoria adaptation task using functional magnetic resonance imaging (MRI) in young adults with normal binocular vision and to test the repeatability of the fMRI measurements for this protocol. The phoria adaptation task consisted of a block protocol of 90 seconds of near visual crossed fixation followed by 90 seconds of far visual uncrossed fixation, repeated three times; the data were collected during two different experimental sessions. Results showed that the oculomotor vermis, cuneus, and primary visual cortex had the greatest functional activity within the regions of interest studied when stimulated by the phoria adaptation task. The oculomotor vermis functional activity had an intraclass correlation coefficient (ICC) of 0.3, whereas the bilateral cuneus and primary visual cortex had good ICC results of greater than 0.6. These results suggest that the sustained visual fixation task described within this study reliably activates the neural substrates of phoria adaptation. This protocol establishes a methodology that can be used in future longitudinal studies investigating therapeutic interventions that may modify phoria adaptation.
G. Elliott Wimmer; Yunzhe Liu; Neža Vehar; Timothy E. J. Behrens; Raymond J. Dolan
Episodic memory retrieval success is associated with rapid replay of episode content Journal Article
In: Nature Neuroscience, vol. 23, no. 8, pp. 1025–1033, 2020.
Retrieval of everyday experiences is fundamental for informing our future decisions. The fine-grained neurophysiological mechanisms that support such memory retrieval are largely unknown. We studied participants who first experienced, without repetition, unique multicomponent 40–80-s episodes. One day later, they engaged in cued retrieval of these episodes while undergoing magnetoencephalography. By decoding individual episode elements, we found that trial-by-trial successful retrieval was supported by the sequential replay of episode elements, with a temporal compression factor of >60. The direction of replay supporting retrieval, either backward or forward, depended on whether the task goal was to retrieve elements of an episode that followed or preceded, respectively, a retrieval cue. This sequential replay was weaker in very-high-performing participants, in whom instead we found evidence for simultaneous clustered reactivation. Our results demonstrate that memory-mediated decisions are supported by a rapid replay mechanism that can flexibly shift in direction in response to task goals.
Niklas Wilming; Peter R. Murphy; Florent Meyniel; Tobias H. Donner
Large-scale dynamics of perceptual decision information across human cortex Journal Article
In: Nature Communications, vol. 11, pp. 5109, 2020.
Perceptual decisions entail the accumulation of sensory evidence for a particular choice towards an action plan. An influential framework holds that sensory cortical areas encode the instantaneous sensory evidence and downstream, action-related regions accumulate this evidence. The large-scale distribution of this computation across the cerebral cortex has remained largely elusive. Here, we develop a regionally-specific magnetoencephalography decoding approach to exhaustively map the dynamics of stimulus- and choice-specific signals across the human cortical surface during a visual decision. Comparison with the evidence accumulation dynamics inferred from behavior disentangles stimulus-dependent and endogenous components of choice-predictive activity across the visual cortical hierarchy. We find such an endogenous component in early visual cortex (including V1), which is expressed in a low (<20 Hz) frequency band and tracks, with delay, the build-up of choice-predictive activity in (pre-) motor regions. Our results are consistent with choice- and frequency-specific cortical feedback signaling during decision formation.
Eelke Spaak; Floris P. Lange
Hippocampal and prefrontal theta-band mechanisms underpin implicit spatial context learning Journal Article
In: Journal of Neuroscience, vol. 40, no. 1, pp. 191–202, 2020.
Humans can rapidly and seemingly implicitly learn to predict typical locations of relevant items when those items are encountered in familiar spatial contexts. Two important questions remain, however, concerning this type of learning: (1) which neural structures and mechanisms are involved in acquiring and exploiting such contextual knowledge? (2) Is this type of learning truly implicit and unconscious? We now answer both these questions after closely examining behavior and recording neural activity using MEG while observers (male and female) were acquiring and exploiting statistical regularities. Computational modeling of behavioral data suggested that, after repeated exposures to a spatial context, participants' behavior was marked by an abrupt switch to an exploitation strategy of the learnt regularities. MEG recordings showed that hippocampus and prefrontal cortex (PFC) were involved in the task and furthermore revealed a striking dissociation: only the initial learning phase was associated with hippocampal theta band activity, while the subsequent exploitation phase showed a shift in theta band activity to the PFC. Intriguingly, the behavioral benefit of repeated exposures to certain scenes was inversely related to explicit awareness of such repeats, demonstrating the implicit nature of the expectations acquired. Together, these findings demonstrate that (1a) hippocampus and PFC play complementary roles in the implicit, unconscious learning and exploitation of spatial statistical regularities; (1b) these mechanisms are implemented in the theta frequency band; and (2) contextual knowledge can indeed be acquired unconsciously, and awareness of such knowledge can even interfere with the exploitation thereof.
L. Tankelevitch; E. Spaak; M. F. S. Rushworth; M. G. Stokes
Previously reward-associated stimuli capture spatial attention in the absence of changes in the corresponding sensory representations as measured with MEG Journal Article
In: Journal of Neuroscience, vol. 40, no. 26, pp. 5033–5050, 2020.
Studies of selective attention typically consider the role of task goals or physical salience, but recent work has shown that attention can also be captured by previously reward-associated stimuli, even when these are no longer relevant (i.e., value-driven attentional capture; VDAC). We used magnetoencephalography (MEG) to investigate how previously reward-associated stimuli are processed, the time-course of reward history effects, and how this relates to the behavioural effects of VDAC. Male and female human participants first completed a reward learning task to establish stimulus-reward associations. Next, we measured attentional capture in a separate task by presenting these stimuli in the absence of reward contingency, and probing their effects on the processing of separate target stimuli presented at different time lags. Using time-resolved multivariate pattern analysis, we found that learned value modulated the spatial selection of previously rewarded stimuli in occipital, inferior temporal, and parietal cortex from $sim$260ms after stimulus onset. This value modulation was related to the strength of participants' behavioural VDAC effect and persisted into subsequent target processing. Furthermore, we found a spatially invariant value signal from $sim$340ms. Importantly, learned value did not influence the neural discriminability of the previously rewarded stimuli in visual cortical areas. Our results suggest that VDAC is underpinned by learned value signals which modulate spatial selection throughout posterior visual and parietal cortex. We further suggest that VDAC can occur in the absence of changes in early visual cortical processing. Significance statement Attention is our ability to focus on relevant information at the expense of irrelevant information. It can be affected by previously learned but currently irrelevant stimulus-reward associations, a phenomenon termed “value-driven attentional capture” (VDAC). The neural mechanisms underlying VDAC remain unclear. It has been speculated that reward learning induces visual cortical plasticity which modulates early visual processing to capture attention. Although we find that learned value modulates spatial attention in sensory brain areas, an effect which correlates with VDAC, we find no relevant signatures of visual cortical plasticity.
Davide Tabarelli; Christian Keitel; Joachim Gross; Daniel Baldauf
Spatial attention enhances cortical tracking of quasi-rhythmic visual stimuli Journal Article
In: NeuroImage, vol. 208, pp. 116444, 2020.
Successfully interpreting and navigating our natural visual environment requires us to track its dynamics constantly. Additionally, we focus our attention on behaviorally relevant stimuli to enhance their neural processing. Little is known, however, about how sustained attention affects the ongoing tracking of stimuli with rich natural temporal dynamics. Here, we used MRI-informed source reconstructions of magnetoencephalography (MEG) data to map to what extent various cortical areas track concurrent continuous quasi-rhythmic visual stimulation. Further, we tested how top-down visuo-spatial attention influences this tracking process. Our bilaterally presented quasi-rhythmic stimuli covered a dynamic range of 4–20 Hz, subdivided into three distinct bands. As an experimental control, we also included strictly rhythmic stimulation (10 vs 12 Hz). Using a spectral measure of brain-stimulus coupling, we were able to track the neural processing of left vs. right stimuli independently, even while fluctuating within the same frequency range. The fidelity of neural tracking depended on the stimulation frequencies, decreasing for higher frequency bands. Both attended and non-attended stimuli were tracked beyond early visual cortices, in ventral and dorsal streams depending on the stimulus frequency. In general, tracking improved with the deployment of visuo-spatial attention to the stimulus location. Our results provide new insights into how human visual cortices process concurrent dynamic stimuli and provide a potential mechanism – namely increasing the temporal precision of tracking – for boosting the neural representation of attended input.
Dillan J. Newbold; Timothy O. Laumann; Catherine R. Hoyt; Jacqueline M. Hampton; David F. Montez; Ryan V. Raut; Mario Ortega; Anish Mitra; Ashley N. Nielsen; Derek B. Miller; Babatunde Adeyemo; Annie L. Nguyen; Kristen M. Scheidter; Aaron B. Tanenbaum; Andrew N. Van; Scott Marek; Bradley L. Schlaggar; Alexandre R. Carter; Deanna J. Greene; Evan M. Gordon; Marcus E. Raichle; Steven E. Petersen; Abraham Z. Snyder; Nico U. F. Dosenbach
Plasticity and spontaneous activity pulses in disused human brain circuits Journal Article
In: Neuron, vol. 107, no. 3, pp. 580–589.e6, 2020.
To induce brain plasticity in humans, we casted the dominant upper extremity for 2 weeks and tracked changes in functional connectivity using daily 30-min scans of resting-state functional MRI (rs-fMRI). Casting caused cortical and cerebellar regions controlling the disused extremity to functionally disconnect from the rest of the somatomotor system, while internal connectivity within the disused sub-circuit was maintained. Functional disconnection was evident within 48 h, progressed throughout the cast period, and reversed after cast removal. During the cast period, large, spontaneous pulses of activity propagated through the disused somatomotor sub-circuit. The adult brain seems to rely on regular use to maintain its functional architecture. Disuse-driven spontaneous activity pulses may help preserve functionally disconnected sub-circuits.
Masih Rahmati; Kevin DeSimone; Clayton E. Curtis; Kartik K. Sreenivasan
Spatially-specific working memory activity in the human superior colliculus Journal Article
In: Journal of Neuroscience, vol. 40, no. 49, pp. 9487–9495, 2020.
Theoretically, working memory (WM) representations are encoded by population activity of neurons with distributed tuning across the stored feature. Here, we leverage computational neuroimaging approaches to map the topographic organization of human superior colliculus (SC) and model how population activity in SC encodes WM representations. We first modeled receptive field properties of voxels in SC, deriving a detailed topographic organization resembling that of the primate SC. Neural activity within human (5 male and 1 female) SC persisted throughout a retention interval of several types of modified memory-guided saccade tasks. Assuming an underlying neural architecture of the SC based on its retinotopic organization, we used an encoding model to show that the pattern of activity in human SC represents locations stored in WM. Our tasks and models allowed us to dissociate the locations of visual targets and the motor metrics of memory-guided saccades from the spatial locations stored in WM, thus confirming that human SC represents true WM information. These data have several important implications. They add the SC to a growing number of cortical and subcortical brain areas that form distributed networks supporting WM functions. Moreover, they specify a clear neural mechanism by which topographically organized SC encodes WM representations.
Zvi N. Roth; Minyoung Ryoo; Elisha P. Merriam
Task-related activity in human visual cortex Journal Article
In: PLoS Biology, vol. 18, no. 11, pp. 1–28, 2020.
The brain exhibits widespread endogenous responses in the absence of visual stimuli, even at the earliest stages of visual cortical processing. Such responses have been studied in monkeys using optical imaging with a limited field of view over visual cortex. Here, we used functional MRI (fMRI) in human participants to study the link between arousal and endogenous responses in visual cortex. The response that we observed was tightly entrained to task timing, was spatially extensive, and was independent of visual stimulation. We found that this response follows dynamics similar to that of pupil size and heart rate, suggesting that task-related activity is related to arousal. Finally, we found that higher reward increased response amplitude while decreasing its trial-To-Trial variability (i.e., the noise). Computational simulations suggest that increased temporal precision underlies both of these observations. Our findings are consistent with optical imaging studies in monkeys and support the notion that arousal increases precision of neural activity.
Tom Salomon; Rotem Botvinik-Nezer; Shiran Oren; Tom Schonberg
Enhanced striatal and prefrontal activity is associated with individual differences in nonreinforced preference change for faces Journal Article
In: Human Brain Mapping, vol. 41, no. 4, pp. 1043–1060, 2020.
Developing effective preference modification paradigms is crucial to improve the quality of life in a wide range of behaviors. The cue-approach training (CAT) paradigm has been introduced as an effective tool to modify preferences lasting months, without external reinforcements, using the mere association of images with a cue and a speeded button response. In the current work for the first time, we used fMRI with faces as stimuli in the CAT paradigm, focusing on face-selective brain regions. We found a behavioral change effect of CAT with faces immediately and 1-month after training, however face-selective regions were not indicative of behavioral change and thus preference change is less likely to rely on face processing brain regions. Nevertheless, we found that during training, fMRI activations in the ventral striatum were correlated with individual preference change. We also found a correlation between preference change and activations in the ventromedial prefrontal cortex during the binary choice phase. Functional connectivity among striatum, prefrontal regions, and high-level visual regions was also related to individual preference change. Our work sheds new light on the involvement of neural mechanisms in the process of valuation. This could lead to development of novel real-world interventions.
Alexandre Sayal; Teresa Sousa; João V. Duarte; Gabriel N. Costa; Ricardo Martins; Miguel Castelo-Branco
Identification of competing neural mechanisms underlying positive and negative perceptual hysteresis in the human visual system Journal Article
In: NeuroImage, vol. 221, pp. 117153, 2020.
Hysteresis is a well-known phenomenon in physics that relates changes in a system with its prior history. It is also part of human visual experience (perceptual hysteresis), and two different neural mechanisms might explain it: persistence (a cause of positive hysteresis), which forces to keep a current percept for longer, and adaptation (a cause of negative hysteresis), which in turn favors the switch to a competing percept early on. In this study, we explore the neural correlates underlying these mechanisms and the hypothesis of their competitive balance, by combining behavioral assessment with fMRI. We used machine learning on the behavioral data to distinguish between positive and negative hysteresis, and discovered a neural correlate of persistence at a core region of the ventral attention network, the anterior insula. Our results add to the understanding of perceptual multistability and reveal a possible mechanistic explanation for the regulation of different forms of perceptual hysteresis.
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.
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.
Constanze Schmitt; Bianca R. Baltaretu; J. Douglas Crawford; Frank Bremmer
A causal role of area hMST for self-motion perception in humans Journal Article
In: Cerebral Cortex Communications, pp. 1–14, 2020.
Previous studies in the macaque monkey have provided clear causal evidence for an involvement of the medial-superior-temporal area (MST) in the perception of self-motion. These studies also revealed an overrepresentation of contraversive heading. Human imaging studies have identified a functional equivalent (hMST) of macaque area MST. Yet, causal evidence of hMST in heading perception is lacking. We employed neuronavigated transcranial magnetic stimulation (TMS) to test for such a causal relationship. We expected TMS over hMST to induce increased perceptual variance (i.e., impaired precision), while leaving mean heading perception (accuracy) unaffected. We presented 8 human participants with an optic flow stimulus simulating forward self-motion across a ground plane in one of 3 directions. Participants indicated perceived heading. In 57% of the trials, TMS pulses were applied, temporally centered on self-motion onset. TMS stimulation site was either right-hemisphere hMST, identified by a functional magnetic resonance imaging (fMRI) localizer, or a control-area, just outside the fMRI localizer activation. As predicted, TMS over area hMST, but not over the control-area, increased response variance of perceived heading as compared with noTMS stimulation trials. As hypothesized, this effect was strongest for contraversive self-motion. These data provide a first causal evidence for a critical role of hMST in visually guided navigation.
Rebekka Schröder; Anna-Maria Kasparbauer; Inga Meyhöfer; Maria Steffens; Peter Trautner; Ulrich Ettinger
Functional connectivity during smooth pursuit eye movements Journal Article
In: Journal of Neurophysiology, vol. 124, pp. 1839–1856, 2020.
Smooth pursuit eye movements (SPEM) hold the image of a slowly moving stimulus on the fovea. The neural system underlying SPEM primarily includes visual, parietal and frontal areas. In the present study, we investigated how these areas are functionally coupled and how these couplings are influenced by target motion frequency. To this end, healthy participants (N=57) were instructed to follow a sinusoidal target stimulus moving horizontally at two different frequencies (0.2 Hz, 0.4 Hz). Eye movements and BOLD activity were recorded simultaneously. Functional connectivity of the key areas of the SPEM network was investigated using a Psychophysiological Interaction (PPI) approach. It was analyzed how activity in five eye movement related seed regions (lateral geniculate nucleus, V1, V5, posterior parietal cortex, frontal eye fields) relates to activity in other parts of the brain during SPEM. The behavioral results showed clear deterioration of SPEM performance at higher target frequency. BOLD activity during SPEM vs. fixation occurred in a geniculo-occipito-parieto-frontal network, replicating previous findings. PPI analysis yielded wide-spread, partially overlapping networks. Especially frontal eye fields and posterior parietal cortex showed task-dependent connectivity to large parts of the entire cortex, while other seed regions demonstrated more regionally focused connectivity. Higher target frequency was associated with stronger activations in visual areas but had no effect on functional connectivity. In summary, the results confirm and extend previous knowledge regarding the neural mechanisms underlying SPEM and provide a valuable basis for further investigations such as in patients with SPEM impairments and known alterations in brain connectivity.
Sarah Schuster; Stefan Hawelka; Nicole Alexandra Himmelstoss; Fabio Richlan; Florian Hutzler
The neural correlates of word position and lexical predictability during sentence reading: Evidence from fixation-related fMRI Journal Article
In: Language, Cognition and Neuroscience, vol. 35, no. 5, pp. 613–624, 2020.
By means of combining eye-tracking and fMRI, the present study aimed to investigate aspects of higher linguistic processing during natural reading which were formerly hard to assess with traditional paradigms. Specifically, we investigated the haemodynamic effects of incremental sentence comprehension–as operationalised by word position–and its relation to context-based word-level effects of lexical predictability. We observed that an increasing amount of words being processed was associated with an increase in activation in the left posterior middle temporal and angular gyri. At the same time, left occipito-temporal regions showed a decrease in activation with increasing word position. Region of interest (ROI) analyses revealed differential effects of word position and predictability within dissociable parts of the semantic network–showing that it is expedient to consider these effects conjointly.
Simon R. Steinkamp; Simone Vossel; Gereon R. Fink; Ralph Weidner
Attentional reorientation along the meridians of the visual field: Are there different neural mechanisms at play? Journal Article
In: Human Brain Mapping, vol. 41, no. 13, pp. 3765–3780, 2020.
Hemispatial neglect, after unilateral lesions to parietal brain areas, is characterized by an inability to respond to unexpected stimuli in contralesional space. As the visual field's horizontal meridian is most severely affected, the brain networks controlling visuospatial processes might be tuned explicitly to this axis. We investigated such a potential directional tuning in the dorsal and ventral frontoparietal attention networks, with a particular focus on attentional reorientation. We used an orientation-discrimination task where a spatial precue indicated the target position with 80% validity. Healthy participants (n = 29) performed this task in two runs and were required to (re-)orient attention either only along the horizontal or the vertical meridian, while fMRI and behavioral measures were recorded. By using a general linear model for behavioral and fMRI data, dynamic causal modeling for effective connectivity, and other predictive approaches, we found strong statistical evidence for a reorientation effect for horizontal and vertical runs. However, neither neural nor behavioral measures differed between vertical and horizontal reorienting. Moreover, models from one run successfully predicted the cueing condition in the respective other run. Our results suggest that activations in the dorsal and ventral attention networks represent higher-order cognitive processes related to spatial attentional (re-)orientating that are independent of directional tuning and that unilateral attention deficits after brain damage are based on disrupted interactions between higher-level attention networks and sensory areas.
Emily R. Stern; Carina Brown; Molly Ludlow; Rebbia Shahab; Katherine Collins; Alexis Lieval; Russell H. Tobe; Dan V. Iosifescu; Katherine E. Burdick; Lazar Fleysher
The buildup of an urge in obsessive–compulsive disorder: Behavioral and neuroimaging correlates Journal Article
In: Human Brain Mapping, vol. 41, no. 6, pp. 1611–1625, 2020.
Obsessive–compulsive disorder (OCD) is highly heterogeneous. While obsessions often involve fear of harm, many patients report uncomfortable sensations and/or urges that drive repetitive behaviors in the absence of a specific fear. Prior work suggests that urges in OCD may be similar to everyday “urges-for-action” (UFA) such as the urge to blink, swallow, or scratch, but very little work has investigated the pathophysiology underlying urges in OCD. In the current study, we used an urge-to-blink approach to model sensory-based urges that could be experimentally elicited and compared across patients and controls using the same task stimuli. OCD patients and controls suppressed eye blinking over a period of 60 s, alternating with free blinking blocks, while brain activity was measured using functional magnetic resonance imaging. OCD patients showed significantly increased activation in several regions during the early phase of eyeblink suppression (first 30 s), including mid-cingulate, insula, striatum, parietal cortex, and occipital cortex, with lingering group differences in parietal and occipital regions during late eyeblink suppression (last 30 s). There were no differences in brain activation during free blinking blocks, and no conditions where OCD patients showed reduced activation compared to controls. In an exploratory analysis of blink counts performed in a subset of subjects, OCD patients were less successful than controls in suppressing blinks. These data indicate that OCD patients exhibit altered brain function and behavior when experiencing and suppressing the urge to blink, raising the possibility that the disorder is associated with a general abnormality in the UFA system that could ultimately be targeted by future treatments.
Susanne Stoll; Nonie J. Finlayson; D. Samuel Schwarzkopf
Topographic signatures of global object perception in human visual cortex Journal Article
In: NeuroImage, vol. 220, pp. 116926, 2020.
Our visual system readily groups dynamic fragmented input into global objects. How the brain represents global object perception remains however unclear. To address this question, we recorded brain responses using functional magnetic resonance imaging whilst observers viewed a dynamic bistable stimulus that could either be perceived globally (i.e., as a grouped and coherently moving shape) or locally (i.e., as ungrouped and incoherently moving elements). We further estimated population receptive fields and used these to back-project the brain activity measured during stimulus perception into visual space via a searchlight procedure. Global perception resulted in universal suppression of responses in lower visual cortex accompanied by wide-spread enhancement in higher object-sensitive cortex. However, follow-up experiments indicated that higher object-sensitive cortex is suppressed if global perception lacks shape grouping, and that grouping-related suppression can be diffusely confined to stimulated sites and accompanied by background enhancement once stimulus size is reduced. These results speak to a non-generic involvement of higher object-sensitive cortex in perceptual grouping and point to an enhancement-suppression mechanism mediating the perception of figure and ground.
Tobias Talanow; Anna-Maria Kasparbauer; Julia V. Lippold; Bernd Weber; Ulrich Ettinger
Neural correlates of proactive and reactive inhibition of saccadic eye movements Journal Article
In: Brain Imaging and Behavior, vol. 14, no. 1, pp. 72–88, 2020.
Although research on goal-directed, proactive inhibitory control (IC) and stimulus-driven, reactive IC is growing, no previous study has compared proactive IC in conditions of uncertainty with regard to upcoming inhibition to conditions of certain upcoming IC. Therefore, we investigated effects of certainty and uncertainty on behavior and blood oxygen level dependent (BOLD) signal in proactive and reactive IC. In two studies, healthy adults performed saccadic go/no-go and prosaccade/antisaccade tasks. The certainty manipulation had a highly significant behavioral effect in both studies, with inhibitory control being more successful under certain than uncertain conditions on both tasks (p ≤ 0.001). Saccadic go responses were significantly less efficient under conditions of uncertainty than certain responding (p < 0.001). Event-related functional magnetic resonance imaging (fMRI) (one study) revealed a dissociation of certainty- and uncertainty-related proactive inhibitory neural correlates in the go/no-go task, with lateral and medial prefrontal and occipital cortex showing stronger deactivations during uncertainty than during certain upcoming inhibition, and lateral parietal cortex being activated more strongly during certain upcoming inhibition than uncertainty or certain upcoming responding. In the antisaccade task, proactive BOLD effects arose due to stronger deactivations in uncertain response conditions of both tasks and before certain prosaccades than antisaccades. Reactive inhibition-related BOLD increases occurred in inferior parietal cortex and supramarginal gyrus (SMG) in the go/no-go task only. Proactive IC may imply focusing attention on the external environment for encoding salient or alerting events as well as inhibitory mechanisms that reduce potentially distracting neural processes. SMG and inferior parietal cortex may play an important role in both proactive and reactive IC of saccades.
Clément Tarrano; Nicolas Wattiez; Cécile Delorme; Eavan M. McGovern; Vanessa Brochard; Stéphane Thobois; Christine Tranchant; David Grabli; Bertrand Degos; Jean Christophe Corvol; Jean Michel Pedespan; Pierre Krystkoviak; Jean Luc Houeto; Adrian Degardin; Luc Defebvre; Romain Valabrègue; Marie Vidailhet; Pierre Pouget; Emmanuel Roze; Yulia Worbe
Visual sensory processing is altered in myoclonus dystonia Journal Article
In: Movement Disorders, vol. 35, no. 1, pp. 151–160, 2020.
Background: Abnormal sensory processing, including temporal discrimination threshold, has been described in various dystonic syndromes. Objective: To investigate visual sensory processing in DYT-SGCE and identify its structural correlates. Methods: DYT-SGCE patients without DBS (DYT-SGCE-non-DBS) and with DBS (DYT-SGCE-DBS) were compared to healthy volunteers in three tasks: a temporal discrimination threshold, a movement orientation discrimination, and movement speed discrimination. Response times attributed to accumulation of sensory visual information were computationally modelized, with $mu$ parameter indicating sensory mean growth rate. We also identified the structural correlates of behavioral performance for temporal discrimination threshold. Results: Twenty-four DYT-SGCE-non-DBS, 13 DYT-SGCE-DBS, and 25 healthy volunteers were included in the study. In DYT-SGCE-DBS, the discrimination threshold was higher in the temporal discrimination threshold (P = 0.024), with no difference among the groups in other tasks. The sensory mean growth rate ($mu$) was lower in DYT-SGCE in all three tasks (P < 0.01), reflecting a slower rate of sensory accumulation for the visual information in these patients independent of DBS. Structural imaging analysis showed a thicker left primary visual cortex (P = 0.001) in DYT-SGCE-non-DBS compared to healthy volunteers, which also correlated with lower $mu$ in temporal discrimination threshold (P = 0.029). In DYT-SGCE-non-DBS, myoclonus severity also correlated with a lower $mu$ in the temporal discrimination threshold task (P = 0.048) and with thicker V1 on the left (P = 0.022). Conclusion: In DYT-SGCE, we showed an alteration of the visual sensory processing in the temporal discrimination threshold that correlated with myoclonus severity and structural changes in the primary visual cortex.
Raphael Vallat; Alain Nicolas; Perrine Ruby
Brain functional connectivity upon awakening from sleep predicts interindividual differences in dream recall frequency Journal Article
In: Sleep, vol. 43, no. 2, pp. 1–11, 2020.
Why do some individuals recall dreams every day while others hardly ever recall one? We hypothesized that sleep inertia—the transient period following awakening associated with brain and cognitive alterations—could be a key mechanism to explain interindividual differences in dream recall at awakening. To test this hypothesis, we measured the brain functional connectivity (combined electroencephalography–functional magnetic resonance imaging) and cognition (memory and mental calculation) of high dream recallers (HR
Johan N. Meer; Michael Breakspear; Luke J. Chang; Saurabh Sonkusare; Luca Cocchi
Movie viewing elicits rich and reliable brain state dynamics Journal Article
In: Nature Communications, vol. 11, pp. 5004, 2020.
Adaptive brain function requires that sensory impressions of the social and natural milieu are dynamically incorporated into intrinsic brain activity. While dynamic switches between brain states have been well characterised in resting state acquisitions, the remodelling of these state transitions by engagement in naturalistic stimuli remains poorly understood. Here, we show that the temporal dynamics of brain states, as measured in fMRI, are reshaped from predominantly bistable transitions between two relatively indistinct states at rest, toward a sequence of well-defined functional states during movie viewing whose transitions are temporally aligned to specific features of the movie. The expression of these brain states covaries with different physiological states and reflects subjectively rated engagement in the movie. In sum, a data-driven decoding of brain states reveals the distinct reshaping of functional network expression and reliable state transitions that accompany the switch from resting state to perceptual immersion in an ecologically valid sensory experience.
Ioannis Agtzidis; Inga Meyhöfer; Michael Dorr; Rebekka Lencer
Following Forrest Gump: Smooth pursuit related brain activation during free movie viewing Journal Article
In: NeuroImage, vol. 216, pp. 116491, 2020.
Most fMRI studies investigating smooth pursuit (SP) related brain activity have used simple synthetic stimuli such as a sinusoidally moving dot. However, real-life situations are much more complex and SP does not occur in isolation but within sequences of saccades and fixations. This raises the question whether the same brain networks for SP that have been identified under laboratory conditions are activated when following moving objects in a movie. Here, we used the publicly available studyforrest data set that provides eye movement recordings along with 3 T fMRI recordings from 15 subjects while watching the Hollywood movie “Forrest Gump”. All three major eye movement events, namely fixations, saccades, and smooth pursuit, were detected with a state-of-the-art algorithm. In our analysis, smooth pursuit (SP) was the eye movement of interest, while saccades were acting as the steady state of viewing behaviour due to their lower variability. For the fMRI analysis we used an event-related design modelling saccades and SP as regressors initially. Because of the interdependency of SP and content motion, we then added a new low-level content motion regressor to separate brain activations from these two sources. We identified higher BOLD-responses during SP than saccades bilaterally in MT+/V5, in middle cingulate extending to precuneus, and in the right temporoparietal junction. When the motion regressor was added, SP showed higher BOLD-response relative to saccades bilaterally in the cortex lining the superior temporal sulcus, precuneus, and supplementary eye field, presumably due to a confounding effect of background motion. Only parts of V2 showed higher activation during saccades in comparison to SP. Taken together, our approach should be regarded as proof of principle for deciphering brain activity related to SP, which is one of the most prominent eye movements besides saccades, in complex dynamic naturalistic situations.
Sara Ajina; Miriam Pollard; Holly Bridge
The superior colliculus and amygdala support evaluation of face trait in blindsight Journal Article
In: Frontiers in Neurology, vol. 11, pp. 769, 2020.
Humans can respond rapidly to viewed expressions of fear, even in the absence of conscious awareness. This is demonstrated using visual masking paradigms in healthy individuals and in patients with cortical blindness due to damage to the primary visual cortex (V1) - so called affective blindsight. Humans have also been shown to implicitly process facial expressions representing important social dimensions. Two major axes, dominance and trustworthiness, are proposed to characterize the social dimensions of face evaluation. The processing of both types of implicit stimuli is believed to occur via similar subcortical pathways involving the amygdala. However, we do not know whether unconscious processing of more subtle expressions of facial traits can occur in blindsight, and if so, how. To test this, we studied 13 patients with unilateral V1 damage and visual field loss. We assessed their ability to detect and discriminate faces that had been manipulated along two orthogonal axes of trustworthiness and dominance to generate five trait levels inside the blind visual field: dominant, submissive, trustworthy, untrustworthy, and neutral. We compared neural activity and functional connectivity in patients classified as blindsight positive or negative for these stimuli. We found that dominant faces were most likely to be detected above chance, with individuals demonstrating unique interactions between performance and face trait. Only patients with blindsight (n = 8) showed significant preference in the superior colliculus and amygdala for face traits in the blind visual field, and a critical functional connection between the amygdala and superior colliculus in the damaged hemisphere. We also found a significant correlation between behavioral performance and fMRI activity in the amygdala and lateral geniculate nucleus across all participants. Our findings confirm that affective blindsight involving the superior colliculus and amygdala extends to the processing of socially salient but emotionally neutral facial expressions when V1 is damaged. This pathway is distinct from that which supports motion blindsight, as both types of blindsight can exist in the absence of the other with corresponding patterns of residual connectivity.
Noor Z. Al Dahhan; John R. Kirby; Ying Chen; Donald C. Brien; Douglas P. Munoz
Examining the neural and cognitive processes that underlie reading through naming speed tasks Journal Article
In: European Journal of Neuroscience, vol. 51, no. 11, pp. 2277–2298, 2020.
We combined fMRI with eye tracking and speech recording to examine the neural and cognitive mechanisms that underlie reading. To simplify the study of the complex processes involved during reading, we used naming speed (NS) tasks (also known as rapid automatized naming or RAN) as a focus for this study, in which average reading right-handed adults named sets of stimuli (letters or objects) as quickly and accurately as possible. Due to the possibility of spoken output during fMRI studies creating motion artifacts, we employed both an overt session and a covert session. When comparing the two sessions, there were no significant differences in behavioral performance, sensorimotor activation (except for regions involved in the motor aspects of speech production) or activation in regions within the left-hemisphere-dominant neural reading network. This established that differences found between the tasks within the reading network were not attributed to speech production motion artifacts or sensorimotor processes. Both behavioral and neuroimaging measures showed that letter naming was a more automatic and efficient task than object naming. Furthermore, specific manipulations to the NS tasks to make the stimuli more visually and/or phonologically similar differentially activated the reading network in the left hemisphere associated with phonological, orthographic and orthographic-to-phonological processing, but not articulatory/motor processing related to speech production. These findings further our understanding of the underlying neural processes that support reading by examining how activation within the reading network differs with both task performance and task characteristics.
Mareike Bacha-Trams; Elisa Ryyppo; Enrico Glerean; Mikko Sams; Iiro P. Jaaskelainen
Social perspective-taking shapes brain hemodynamic activity and eye movements during movie viewing Journal Article
In: Social Cognitive and Affective Neuroscience, vol. 15, no. 2, pp. 175–191, 2020.
Putting oneself into the shoes of others is an important aspect of social cognition.We measured brain hemodynamic activity and eye-gaze patterns while participants were viewing a shortened version of the movie 'My Sister's Keeper' from two perspectives: That of a potential organ donor, who violates moral norms by refusing to donate her kidney, and that of a potential organ recipient, who suffers in pain. Inter-subject correlation (ISC) of brain activity was significantly higher during the potential organ donor's perspective in dorsolateral and inferior prefrontal, lateral and inferior occipital, and inferior-anterior temporal areas. In the reverse contrast, stronger ISC was observed in superior temporal, posterior frontal and anterior parietal areas. Eye-gaze analysis showed higher proportion of fixations on the potential organ recipient during both perspectives. Taken together, these results suggest that during social perspective-taking different brain areas can be flexibly recruited depending on the nature of the perspective that is taken.
Valerie M. Beck; Timothy J. Vickery
Oculomotor capture reveals trial-by-trial neural correlates of attentional guidance by contents of visual working memory Journal Article
In: Cortex, vol. 122, pp. 159–169, 2020.
Evidence from attentional and oculomotor capture, contingent capture, and other paradigms suggests that mechanisms supporting human visual working memory (VWM) and visual attention are intertwined. Features held in VWM bias guidance toward matching items even when those features are task irrelevant. However, the neural basis of this interaction is underspecified. Prior examinations using fMRI have primarily relied on coarse comparisons across experimental conditions that produce varying amounts of capture. To examine the neural dynamics of attentional capture on a trial-by-trial basis, we applied an oculomotor paradigm that produced discrete measures of capture. On each trial, subjects were shown a memory item, followed by a blank retention interval, then a saccade target that appeared to the left or right. On some trials, an irrelevant distractor appeared above or below fixation. Once the saccade target was fixated, subjects completed a forced-choice memory test. Critically, either the target or distractor could match the feature held in VWM. Although task irrelevant, this manipulation produced differences in behavior: participants were more likely to saccade first to an irrelevant VWM-matching distractor compared with a non-matching distractor – providing a discrete measure of capture. We replicated this finding while recording eye movements and scanning participants' brains using fMRI. To examine the neural basis of oculomotor capture, we separately modeled the retention interval for capture and non-capture trials within the distractor-match condition. We found that frontal activity, including anterior cingulate cortex and superior frontal gyrus regions, differentially predicted subsequent oculomotor capture by a memory-matching distractor. Other regions previously implicated as involved in attentional capture by VWM-matching items showed no differential activity across capture and non-capture trials, even at a liberal threshold. Our findings demonstrate the power of trial-by-trial analyses of oculomotor capture as a means to examine the underlying relationship between VWM and attentional guidance systems.