Johannes J. D. Singer; Radoslaw M. Cichy; Martin N. Hebart
The spatiotemporal neural dynamics of object recognition for natural images and line drawings Journal Article
In: Journal of Neuroscience, vol. 43, no. 3, pp. 484–500, 2023.
Drawings offer a simple and efficient way to communicate meaning. While line drawings capture only coarsely how objects look in reality, we still perceive them as resembling real-world objects. Previous work has shown that this perceived similarity is mirrored by shared neural representations for drawings and natural images, which suggests that similar mechanisms underlie the recognition of both. However, other work has proposed that representations of drawings and natural images become similar only after substantial processing has taken place, suggesting distinct mechanisms. To arbitrate between those alternatives, we measured brain responses resolved in space and time using fMRI and MEG, respectively, while human participants (female and male) viewed images of objects depicted as photographs, line drawings, or sketch-like drawings. Using multivariate decoding, we demonstrate that object category information emerged similarly fast and across overlapping regions in occipital, ventral-temporal, and posterior parietal cortex for all types of depiction, yet with smaller effects at higher levels of visual abstraction. In addition, cross-decoding between depiction types revealed strong generalization of object category information from early processing stages on. Finally, by combining fMRI and MEG data using representational similarity analysis, we found that visual information traversed similar processing stages for all types of depiction, yet with an overall stronger representation for photographs. Together, our results demonstrate broad commonalities in the neural dynamics of object recognition across types of depiction, thus providing clear evidence for shared neural mechanisms underlying recognition of natural object images and abstract drawings.
Amir Assouline; Avi Mendelsohn
Weaving a story: Narrative formation over prolonged time scales engages social cognition and frontoparietal networks Journal Article
In: European Journal of Neuroscience, pp. 1–15, 2023.
Forming narratives is of key importance to human experience, enabling one to render large amounts of information into relatively compacted stories for future retrieval, giving meaning to otherwise fragmented occurrences. The neural mechanisms that underlie coherent narrative construction of causally connected information over prolonged temporal periods are yet unclear. Participants in this fMRI study observed consecutive scenes from a full-length movie either in their original order, enabling causal inferences over time, or in reverse order, impeding a key component of coherent narratives—causal inference. In between scenes, we presented short periods of blank screens for examining post-encoding processing effects. Using multivariate pattern analysis (MVPA) followed by seed-base correlation analysis, we hypothesized that net- works involved in online monitoring of incoming information on the one hand, and offline processing of previous occurrences on the other would differ between the groups. We found that despite the exposure to the same scenes, the chronological-order condition exhibited enhanced functional connectivity in frontoparietal regions associated with information integration and working memory. The reverse-order condition yielded offline, post-scene coactivation of neural networks involved in social cognition and particularly theory of mind and action comprehension. These findings shed light on offline processes of narrative construction efforts, highlighting the role of social cognition networks in seeking for narrative coherence.
Nick Fogt; Andrew J Toole; Xiangrui Li; Emmanuel Owusu; Steven T Manning; Marjean T Kulp
Functional magnetic resonance imaging activation for different vergence eye movement subtypes Journal Article
In: Ophthalmic and Physiological Optics, vol. 43, pp. 93–104, 2023.
Introduction: Maddox suggested that there were four convergence subtypes, each driven by a different stimulus. The purpose of this study was to assess the neural correlates for accommodative convergence, proximal convergence (convergence stimulus provided), disparity convergence and voluntary convergence (no specific convergence stimulus provided) using functional magnetic resonance imaging (fMRI). Methods: Ten subjects (mean age = 24.4 years) with normal binocular vision participated. The blood oxygenation level- dependent (BOLD) signals of the brain from fMRI scans were measured when subjects made vergence eye movements while: (1) alternately viewing letters monocularly where one eye viewed through a −2.00 D lens, (2) alternately viewing Difference of Gaussian targets monocularly at distance and near, (3) viewing random dot stereograms with increasing disparity and (4) voluntarily converging the eyes with binocular viewing. Results: The accommodative convergence paradigm resulted in activation on the right side in the right fusiform cortex and the right middle occipital cortex. The proximal convergence stimulus mainly activated areas in the right occipital lobe. The disparity stimulus activated areas in the left occipital cortex and the left frontal cortex. Finally, the voluntary convergence paradigm resulted in activation primarily in the occipital lobe and mostly bilaterally. Conclusion: The accommodative, proximal, disparity and voluntary convergence paradigms resulted in activation in unique areas in the brain with functional MRI. Activation was found in more areas in the proximal and voluntary conditions compared with the accommodative and disparity conditions.
Susana Mouga; Isabel Catarina Duarte; Cátia Café; Daniela Sousa; Frederico Duque; Guiomar Oliveira; Miguel Castelo-Branco
Parahippocampal deactivation and hyperactivation of central executive, saliency and social cognition networks in autism spectrum disorder Journal Article
In: Journal of Neurodevelopmental Disorders, vol. 14, no. 9, pp. 1–12, 2022.
Background: The concomitant role of the Central Executive, the Saliency and the Social Cognition networks in autism spectrum disorder (ASD) in demanding ecological tasks remains unanswered. We addressed this question using a novel task-based fMRI virtual-reality task mimicking a challenging daily-life chore that may present some difficulties to individuals with ASD: the EcoSupermarketX. Methods: Participants included 29 adolescents: 15 with ASD and 15 with typical neurodevelopment (TD). They performed the EcoSupermarketX (a shopping simulation with three goal-oriented sub-tasks including “no cue”, “non-social” or “social” cues), during neuroimaging and eye-tracking. Results: ASD differed from TD only in total time and distance to complete the “social cue” sub-task with matched eye-tracking measures. Neuroimaging revealed simultaneous hyperactivation across social, executive, and saliency circuits in ASD. In contrast, ASD showed reduced activation in the parahippocampal gyrus, involved in scene recognition. Conclusions: When performing a virtual shopping task matching the performance of controls, ASD adolescents hyperactivate three core networks: executive, saliency and social cognition. Parahippocampal hypoactivation is consistent with effortless eidetic scene processing, in line with the notion of peaks and valleys of neural recruitment in individuals with ASD. These hyperactivation/hypoactivation patterns in daily life tasks provide a circuit-level signature of neural diversity in ASD, a possible intervention target.
Jordana S. Wynn; Zhong-Xu Liu; Jennifer D. Ryan
Neural correlates of subsequent memory-related gaze reinstatement Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, no. 9, pp. 1547–1562, 2022.
Mounting evidence linking gaze reinstatement—the recapitulation of encoding-related gaze patterns during retrieval—to behavioral measures of memory suggests that eye movements play an important role in mnemonic processing. Yet, the nature of the gaze scanpath, including its informational content and neural correlates, has remained in question. In this study, we examined eye movement and neural data from a recognition memory task to further elucidate the behavioral and neural bases of functional gaze reinstatement. Consistent with previous work, gaze reinstatement during retrieval of freely viewed scene images was greater than chance and predictive of recognition memory performance. Gaze reinstatement was also associated with viewing of informationally salient image regions at encoding, suggesting that scanpaths may encode and contain high-level scene content. At the brain level, gaze reinstatement was predicted by encoding-related activity in the occipital pole and BG, neural regions associated with visual processing and oculomotor control. Finally, cross-voxel brain pattern similarity analysis revealed overlapping subsequent memory and subsequent gaze reinstatement modulation effects in the parahippocampal place area and hippocampus, in addition to the occipital pole and BG. Together, these findings suggest that encoding-related activity in brain regions associated with scene processing, oculomotor control, and memory supports the formation, and subsequent recapitulation, of functional scanpaths. More broadly, these findings lend support to Scanpath Theory's assertion that eye movements both encode, and are themselves embedded in, mnemonic representations.
Christoph Helmchen; Philipp J. Koch; Gabriel Girard; Norbert Brüggemann; Björn Machner; Andreas Sprenger
NPTX1-related oculomotor apraxia: An intra-hemispheric disconnection disorder Miscellaneous
Oculomotor apraxia (OMA) is a rare and heavily disabling neurological disorder causing severe difficulties in the initia- tion and maintenance of voluntary eye movements when the head is stationary. If patients try to initiate saccades, they are grossly delayed and hypometric (stair-case). .. The aim of this study was to test competing pathophysiological hypotheses by functional and structural MRI, stating that OMA is related to either abnormal (i) inter-hemispheric or (ii) intra-hemispheric connectivity between the FEF and related oculomotor structures (oculomotor network) or (iii) both mechanisms.
Evan M. Gordon; Timothy O. Laumann; Scott Marek; Dillan J. Newbold; Jacqueline M. Hampton; Nicole A. Seider; David F. Montez; Ashley M. Nielsen; Andrew N. Van; Annie Zheng; Ryland Miller; Joshua S. Siegel; Benjamin P. Kay; Abraham Z. Snyder; Deanna J. Greene; Bradley L. Schlaggar; Steven E. Petersen; Steven M. Nelson; Nico U. F. Dosenbach
Individualized functional subnetworks connect human striatum and frontal cortex Journal Article
In: Cerebral Cortex, vol. 32, no. 13, pp. 2868–2884, 2022.
The striatum and cerebral cortex are interconnected via multiple recurrent loops that play a major role in many neuropsychiatric conditions. Primate corticostriatal connections can be precisely mapped using invasive tract-tracing. However, noninvasive human research has not mapped these connections with anatomical precision, limited in part by the practice of averaging neuroimaging data across individuals. Here we utilized highly sampled resting-state functional connectivity MRI for individual-specific precision functional mapping (PFM) of corticostriatal connections. We identified ten individual-specific subnetworks linking cortex—predominately frontal cortex—to striatum, most of which converged with nonhuman primate tract-tracing work. These included separable connections between nucleus accumbens core/shell and orbitofrontal/medial frontal gyrus; between anterior striatum and dorsomedial prefrontal cortex; between dorsal caudate and lateral prefrontal cortex; and between middle/posterior putamen and supplementary motor/primary motor cortex. Two subnetworks that did not converge with nonhuman primates were connected to cortical regions associated with human language function. Thus, precision subnetworks identify detailed, individual-specific, neurobiologically plausible corticostriatal connectivity that includes human-specific language networks.
Marcus Grueschow; Birgit Kleim; Christian Carl Ruff
Functional coupling of the locus coeruleus is linked to successful cognitive control Journal Article
In: Brain Sciences, vol. 12, no. 3, pp. 1–15, 2022.
The locus coeruleus (LC) is a brainstem structure that sends widespread efferent projections throughout the mammalian brain. The LC constitutes the major source of noradrenaline (NE), a modulatory neurotransmitter that is crucial for fundamental brain functions such as arousal, attention, and cognitive control. This role of the LC-NE is traditionally not believed to reflect functional influences on the frontoparietal network or the striatum, but recent advances in chemogenetic manipulations of the rodent brain have challenged this notion. However, demonstrations of LCNE functional connectivity with these areas in the human brain are surprisingly sparse. Here, we close this gap. Using an established emotional stroop task, we directly compared trials requiring response conflict control with trials that did not require this, but were matched for visual stimulus properties, response modality, and controlled for pupil dilation differences across both trial types. We found that LC-NE functional coupling with the parietal cortex and regions of the striatum is substantially enhanced during trials requiring response conflict control. Crucially, the strength of this functional coupling was directly related to individual reaction time differences incurred by conflict resolution. Our data concur with recent rodent findings and highlight the importance of converging evidence between human and nonhuman neurophysiology to further understand the neural systems supporting adaptive and maladaptive behavior in health and disease.
Hengda He; Nabil Ettehadi; Amir Shmuel; Qolamreza R. Razlighi
Evidence suggesting common mechanisms underlie contralateral and ipsilateral negative BOLD responses in the human visual cortex Journal Article
In: NeuroImage, vol. 262, pp. 1–13, 2022.
The task-evoked positive BOLD response (PBR) to a unilateral visual hemi-field stimulation is often accompanied by robust and sustained contralateral as well as ipsilateral negative BOLD responses (NBRs) in the visual cortex. The signal characteristics and the neural and/or vascular mechanisms that underlie these two types of NBRs are not completely understood. In this paper, we investigated the properties of these two types of NBRs. We first demonstrated the linearity of both NBRs with respect to stimulus duration. Next, we showed that the hemodynamic response functions (HRFs) of the two NBRs were similar to each other, but significantly different from that of the PBR. Moreover, the subject-wise expressions of the two NBRs were tightly coupled to the degree that the correlation between the two NBRs was significantly higher than the correlation between each NBR and the PBR. However, the activation patterns of the two NBRs did not show a high level of interhemispheric spatial similarity, and the functional connectivity between them was not different than the interhemispheric functional connectivity between the NBRs and PBR. Finally, while attention did modulate both NBRs, the attention-related changes in their HRFs were similar. Our findings suggest that the two NBRs might be generated through common neural and/or vascular mechanisms involving distal/deep brain regions that project to the two hemispheres.
Juyoen Hur; Manuel Kuhn; Shannon E. Grogans; Allegra S. Anderson; Samiha Islam; Hyung Cho Kim; Rachael M. Tillman; Andrew S. Fox; Jason F. Smith; Kathryn A. DeYoung; Alexander J. Shackman
Anxiety-related frontocortical activity is associated with dampened stressor reactivity in the real world Journal Article
In: Psychological Science, vol. 33, no. 6, pp. 906–924, 2022.
Negative affect is a fundamental dimension of human emotion. When extreme, it contributes to a variety of adverse outcomes, from physical and mental illness to divorce and premature death. Mechanistic work in animals and neuroimaging research in humans and monkeys have begun to reveal the broad contours of the neural circuits governing negative affect, but the relevance of these discoveries to everyday distress remains incompletely understood. Here, we used a combination of approaches—including neuroimaging assays of threat anticipation and emotional-face perception and more than 10,000 momentary assessments of emotional experience—to demonstrate that individuals who showed greater activation in a cingulo-opercular circuit during an anxiety-eliciting laboratory paradigm experienced lower levels of stressor-dependent distress in their daily lives (ns = 202–208 university students). Extended amygdala activation was not significantly related to momentary negative affect. These observations provide a framework for understanding the neurobiology of negative affect in the laboratory and in the real world.
Tarik Jamoulle; Qian Ran; Karen Meersmans; Jolien Schaeverbeke; Patrick Dupont; Rik Vandenberghe
Posterior intraparietal sulcus mediates detection of salient stimuli outside the endogenous focus of attention Journal Article
In: Cerebral Cortex, vol. 32, pp. 1455–1469, 2022.
Visual consciousness is shaped by the interplay between endogenous selection and exogenous capture. If stimulus saliency is aligned with a subject's attentional priorities, endogenous selection will be facilitated. In case of a misalignment, endogenous selection may be compromised as attentional capture is a strong and automatic process. We manipulated task-congruent versus -incongruent saliency in a functional magnetic resonance imaging change-detection task and analyzed brain activity patterns in the cortex surrounding the intraparietal sulcus (IPS) within the Julich-Brain probabilistic cytoarchitectonic mapping reference frame. We predicted that exogenous effects would be seen mainly in the posterior regions of the IPS (hIP4-hIP7-hIP8), whereas a conflict between endogenous and exogenous orienting would elicit activity from more anterior cytoarchitectonic areas (hIP1-hIP2-hIP3). Contrary to our hypothesis, a conflict between endogenous and exogenous orienting had an effect early in the IPS (mainly in hIP7 and hIP8). This is strong evidence for an endogenous component in hIP7/8 responses to salient stimuli beyond effects of attentional bottom-up sweep. Our results suggest that hIP7 and hIP8 are implicated in the individuation of attended locations based on saliency as well as endogenous instructions.
Romuald A. Janik; Igor T. Podolak; Łukasz Struski; Anna Ceglarek; Koryna Lewandowska; Barbara Sikora-Wachowicz; Tadeusz Marek; Magdalena Fafrowicz
Neural spatio-temporal patterns of information processing related to cognitive conflict and correct or false recognitions Journal Article
In: Scientific Reports, vol. 12, no. 1, pp. 1–19, 2022.
Using a visual short-term memory task and employing a new methodological approach, we analyzed neural responses from the perspective of the conflict level and correctness/erroneous over a longer time window. Sixty-five participants performed the short-term memory task in the fMRI scanner. We explore neural spatio-temporal patterns of information processing in the context of correct or erroneous response and high or low level of cognitive conflict using classical fMRI analysis, surface-based cortical data, temporal analysis of interpolated mean activations, and machine learning classifiers. Our results provide evidence that information processing dynamics during the retrieval process vary depending on the correct or false recognition—for stimuli inducing a high level of cognitive conflict and erroneous response, information processing is prolonged. The observed phenomenon may be interpreted as the manifestation of the brain's preparation for future goal-directed action.
Zhenlan Jin; Dong-gang Jin; Min Xiao; Aolin Ding; Jing Tian; Junjun Zhang; Ling Li
Structural and functional MRI evidence for significant contribution of precentral gyrus to flexible oculomotor control: Evidence from the antisaccade task Journal Article
In: Brain Structure and Function, vol. 227, no. 8, pp. 2623–2632, 2022.
Antisaccade task requires inhibition of a prepotent prosaccade to a peripheral target and initiation of a saccade to the opposite location, and, therefore, is used as a tool to investigate behavioral adjustment. The frontal and parietal cortices are both known for their activation during saccade generation, but it is unclear whether their neuroanatomical characteristics also contribute to antisaccades. Here, we took antisaccade cost (antisaccade latency minus prosaccade latency) as an index for additional time for generating antisaccades. Fifty-eight participants conducted pro and antisaccade tasks outside the magnetic resonance imaging (MRI) scanner and their structural MRI (sMRI) data were also collected to explore brain regions neuroanatomically related to antisaccade cost. Then, twelve participants performed saccade tasks in the scanner and their task-state functional MRI (fMRI) data were collected to verify the activation of structurally identified brain regions during the saccade generation. Voxel-based morphometry (VBM) results revealed that gray matter volume (GMV) of the left precentral gyrus and the left insula were positively correlated with the antisaccade cost, which was validated by the prediction analysis. Brain activation results showed the activation of the precentral during both pro and antisaccade execution period, but not the insula. Our results suggest that precentral gyrus and insula play vital roles to antisaccade cost, but possibly in different ways. The insula, a key node of the salience network, possibly regulates the saliency processing of the target, while the precentral gyrus possibly mediates the generation of saccades. Our study especially highlights an outstanding role of the precentral gyrus in flexible oculomotor control.
Johannes Kirchner; Tamara Watson; Markus Lappe
Real-time MRI reveals unique insight into the full eye kinematics of eye movements Journal Article
In: eNeuro, vol. 9, no. 1, pp. 1–14, 2022.
Our eyes are constantly in motion and the various kinds of eye movements are closely linked to many aspects of human cognitive processing. Measuring all possible eye movements unobtrusively is not achievable with current methods. Video-based eye-trackers only measure rotational but not translational motion of the eye, re- quire a calibration process relying on the participant's self-report of accurate fixation, and do not work if vision of the eyeball is blocked. Scleral search coils attach physical weight on the eyeball and also do not measure translation. Here, we describe a novel and fully automated method to use real-time magnetic resonance imaging (MRI) for eye tracking. We achieved a temporal resolution sufficient to measure eye rotations and transla- tions as short as those that occur within a blink and behind a closed eyelid. To demonstrate this method, we measured the full extent of the blink-related eye movement for two individuals, suggesting that the eye approaches a holding position during lid closure and can move by as much as 35° in rotation and 2 mm in translation. We also investigated the coordination of gaze shifts with blinks. We found that the gaze shift is tightly coupled in time to the translational blink movement and that blinks can induce significant temporal shifts of the gaze trajectory between left and right eye. Our MR-based Eye Tracking (MREyeTrack) method allows measurement of eye movements in terms of both translation and rotation and enables new opportunities for study- ing ocular motility and its disorders.
Sharif I. Kronemer; Mark Aksen; Julia Z. Ding; Jun Hwan Ryu; Qilong Xin; Zhaoxiong Ding; Jacob S. Prince; Hunki Kwon; Aya Khalaf; Sarit Forman; David S. Jin; Kevin Wang; Kaylie Chen; Claire Hu; Akshar Agarwal; Erik Saberski; Syed Mohammad Adil Wafa; Owen P. Morgan; Jia Wu; Kate L. Christison-Lagay; Nicholas Hasulak; Martha Morrell; Alexandra Urban; R. Todd Constable; Michael Pitts; R. Mark Richardson; Michael J. Crowley; Hal Blumenfeld
Human visual consciousness involves large scale cortical and subcortical networks independent of task report and eye movement activity Journal Article
In: Nature Communications, vol. 13, pp. 1–17, 2022.
The full neural circuits of conscious perception remain unknown. Using a visual perception task, we directly recorded a subcortical thalamic awareness potential (TAP). We also developed a unique paradigm to classify perceived versus not perceived stimuli using eye measurements to remove confounding signals related to reporting on conscious experiences. Using fMRI, we discovered three major brain networks driving conscious visual perception independent of report: first, increases in signal detection regions in visual, fusiform cortex, and frontal eye fields; and in arousal/salience networks involving midbrain, thalamus, nucleus accumbens, anterior cingulate, and anterior insula; second, increases in frontoparietal attention and executive control networks and in the cerebellum; finally, decreases in the default mode network. These results were largely maintained after excluding eye movement-based fMRI changes. Our findings provide evidence that the neurophysiology of consciousness is complex even without overt report, involving multiple cortical and subcortical networks overlapping in space and time.
Kiri Kuroda; Yukiko Ogura; Akitoshi Ogawa; Tomoya Tamei; Kazushi Ikeda; Tatsuya Kameda
Behavioral and neuro-cognitive bases for emergence of norms and socially shared realities via dynamic interaction Journal Article
In: Communications Biology, vol. 5, no. 1, pp. 1–13, 2022.
In the digital era, new socially shared realities and norms emerge rapidly, whether they are beneficial or harmful to our societies. Although these are emerging properties from dynamic interaction, most research has centered on static situations where isolated individuals face extant norms. We investigated how perceptual norms emerge endogenously as shared realities through interaction, using behavioral and fMRI experiments coupled with computational modeling. Social interactions fostered convergence of perceptual responses among people, not only overtly but also at the covert psychophysical level that generates overt responses. Reciprocity played a critical role in increasing the stability (reliability) of the psychophysical function within each individual, modulated by neural activity in the mentalizing network during interaction. These results imply that bilateral influence promotes mutual cognitive anchoring of individual views, producing shared generative models at the collective level that enable endogenous agreement on totally new targets–one of the key functions of social norms.
Natalia Ladyka-Wojcik; Zhong-Xu Liu; Jennifer D. Ryan
Unrestricted eye movements strengthen effective connectivity from hippocampal to oculomotor regions during scene construction Journal Article
In: NeuroImage, vol. 260, pp. 1–15, 2022.
Scene construction is a key component of memory recall, navigation, and future imagining, and relies on the medial temporal lobes (MTL). A parallel body of work suggests that eye movements may enable the imagination and construction of scenes, even in the absence of external visual input. There are vast structural and functional connections between regions of the MTL and those of the oculomotor system. However, the directionality of connections between the MTL and oculomotor control regions, and how it relates to scene construction, has not been studied directly in human neuroimaging. In the current study, we used dynamic causal modeling (DCM) to interrogate effective connectivity between the MTL and oculomotor regions using a scene construction task in which participants' eye movements were either restricted (fixed-viewing) or unrestricted (free-viewing). By omitting external visual input, and by contrasting free- versus fixed- viewing, the directionality of neural connectivity during scene construction could be determined. As opposed to when eye movements were restricted, allowing free-viewing during construction of scenes strengthened top-down connections from the MTL to the frontal eye fields, and to lower-level cortical visual processing regions, suppressed bottom-up connections along the visual stream, and enhanced vividness of the constructed scenes. Taken together, these findings provide novel, non-invasive evidence for the underlying, directional, connectivity between the MTL memory system and oculomotor system associated with constructing vivid mental representations of scenes.
Armien Lanssens; Dante Mantini; Hans Op Beeck; Celine R. Gillebert
Activity in the fronto-parietal and visual cortex is modulated by feature-based attentional weighting Journal Article
In: Frontiers in Neuroscience, vol. 16, pp. 1–15, 2022.
In day-to-day dynamic activities where sensory input is abundant, stimulus representations in the visual cortex are modulated based on their attentional priority. Several studies have established the top-down role of a fronto-parietal dorsal attention network in selective attention. In the current study, we aimed to investigate whether activity of subregions of this network and the visual cortex is modulated by feature-based attentional weighting, and if so, whether their timecourses of activity are correlated. To this end, we analyzed fMRI data of 28 healthy subjects, who performed a feature-based go/no-go task. Participants had to attend to one or two colored streams of sinusoidal gratings and respond to each grating in the task-relevant stream(s) except to a single non-target grating. Univariate and multivariate fMRI results indicated that activity in bilateral fronto-parietal (frontal eye fields, intraparietal sulcus and superior parietal lobe) and visual (V1–V4, lateral occipital cortex and fusiform gyrus) regions was modulated by selecting one instead of attending to two gratings. Functional connectivity was not significantly different between fronto-parietal and visual regions when attending to one as opposed to two gratings. Our study demonstrates that activity in subregions of both the fronto-parietal and visual cortex is modified by feature-based attentional weighting.
Kangjoo Lee; Corey Horien; David O'Connor; Bronwen Garand-Sheridan; Fuyuze Tokoglu; Dustin Scheinost; Evelyn M. R. Lake; R. Todd Constable
Arousal impacts distributed hubs modulating the integration of brain functional connectivity Journal Article
In: NeuroImage, vol. 258, pp. 1–17, 2022.
Even when subjects are at rest, it is thought that brain activity is organized into distinct brain states during which reproducible patterns are observable. Yet, it is unclear how to define or distinguish different brain states. A potential source of brain state variation is arousal, which may play a role in modulating functional interactions between brain regions. Here, we use simultaneous resting state functional magnetic resonance imaging (fMRI) and pupillometry to study the impact of arousal levels indexed by pupil area on the integration of large-scale brain networks. We employ a novel sparse dictionary learning-based method to identify hub regions participating in between-network integration stratified by arousal, by measuring k-hubness, the number (k) of functionally overlapping networks in each brain region. We show evidence of a brain-wide decrease in between-network integration and inter-subject variability at low relative to high arousal, with differences emerging across regions of the frontoparietal, default mode, motor, limbic, and cerebellum networks. State-dependent changes in k-hubness relate to the actual patterns of network integration within these hubs, suggesting a brain state transition from high to low arousal characterized by global synchronization and reduced network overlaps. We demonstrate that arousal is not limited to specific brain areas known to be directly associated with arousal regulation, but instead has a brain-wide impact that involves high-level between-network communications. Lastly, we show a systematic change in pairwise fMRI signal correlation structures in the arousal state-stratified data, and demonstrate that the choice of global signal regression could result in different conclusions in conventional graph theoretical analysis and in the analysis of k-hubness when studying arousal modulations. Together, our results suggest the presence of global and local effects of pupil-linked arousal modulations on resting state brain functional connectivity.
Yih-Shiuan Lin; Chien-Chung Chen; Mark W. Greenlee
Neural correlates of lateral modulation and perceptual filling-in in center-surround radial sinusoidal gratings: An fMRI study Journal Article
In: Scientific Reports, vol. 12, pp. 1–14, 2022.
We investigated lateral modulation effects with functional magnetic resonance imaging. We presented radial sinusoidal gratings in random sequence: a scotoma grating with two arc-shaped blank regions (scotomata) in the periphery, one in the left and one in the right visual field, a center grating containing pattern only in the scotoma regions, and a full-field grating where the pattern occupied the whole screen. On each trial, one of the three gratings flickered in counterphase for 10 s, followed by a blank period. Observers were instructed to perform a fixation task and report whether filling-in was experienced during the scotoma condition. The results showed that the blood-oxygen-level-dependent signal was reduced in areas corresponding to the scotoma regions in the full-field compared to the center condition in V1 to V3 areas, indicating a lateral inhibition effect when the surround was added to the center pattern. The univariate analysis results showed no difference between the filling-in and no-filling-in trials. However, multivariate pattern analysis results showed that classifiers trained on activation pattern in V1 to V3 could differentiate between filling-in and no-filling-in trials, suggesting that the neural activation pattern in visual cortex correlated with the subjective percept.
Christina Lubinus; Wolfgang Einhäuser; Florian Schiller; Tilo Kircher; Benjamin Straube; Bianca M. Kemenade
Action-based predictions affect visual perception, neural processing, and pupil size, regardless of temporal predictability Journal Article
In: NeuroImage, vol. 263, pp. 1–13, 2022.
Sensory consequences of one's own action are often perceived as less intense, and lead to reduced neural responses, compared to externally generated stimuli. Presumably, such sensory attenuation is due to predictive mechanisms based on the motor command (efference copy). However, sensory attenuation has also been observed outside the context of voluntary action, namely when stimuli are temporally predictable. Here, we aimed at disentangling the effects of motor and temporal predictability-based mechanisms on the attenuation of sensory action consequences. During fMRI data acquisition, participants (N = 25) judged which of two visual stimuli was brighter. In predictable blocks, the stimuli appeared temporally aligned with their button press (active) or aligned with an automatically generated cue (passive). In unpredictable blocks, stimuli were presented with a variable delay after button press/cue, respectively. Eye tracking was performed to investigate pupil-size changes and to ensure proper fixation. Self-generated stimuli were perceived as darker and led to less neural activation in visual areas than their passive counterparts, indicating sensory attenuation for self-generated stimuli independent of temporal predictability. Pupil size was larger during self-generated stimuli, which correlated negatively with the blood oxygenation level dependent (BOLD) response: the larger the pupil, the smaller the BOLD amplitude in visual areas. Our results suggest that sensory attenuation in visual cortex is driven by action-based predictive mechanisms rather than by temporal predictability. This effect may be related to changes in pupil diameter. Altogether, these results emphasize the role of the efference copy in the processing of sensory action consequences.
Björn Machner; Lara Braun; Jonathan Imholz; Philipp J. Koch; Thomas F. Münte; Christoph Helmchen; Andreas Sprenger
Resting-state functional connectivity in the dorsal attention network relates to behavioral performance in spatial attention tasks and may show task-related adaptation Journal Article
In: Frontiers in Human Neuroscience, vol. 15, pp. 1–12, 2022.
Between-subject variability in cognitive performance has been related to inter-individual differences in functional brain networks. Targeting the dorsal attention network (DAN) we questioned (i) whether resting-state functional connectivity (FC) within the DAN can predict individual performance in spatial attention tasks and (ii) whether there is short-term adaptation of DAN-FC in response to task engagement. Twenty-seven participants first underwent resting-state fMRI (PRE run), they subsequently performed different tasks of spatial attention [including visual search (VS)] and immediately afterwards received another rs-fMRI (POST run). Intra- and inter-hemispheric FC between core hubs of the DAN, bilateral intraparietal sulcus (IPS) and frontal eye field (FEF), was analyzed and compared between PRE and POST. Furthermore, we investigated rs-fMRI-behavior correlations between the DAN-FC in PRE/POST and task performance parameters. The absolute DAN-FC did not change from PRE to POST. However, different significant rs-fMRI-behavior correlations were revealed for intra-/inter-hemispheric connections in the PRE and POST run. The stronger the FC between left FEF and IPS before task engagement, the better was the learning effect (improvement of reaction times) in VS (r = 0.521
Paola Mengotti; Anne Sophie Käsbauer; Gereon R. Fink; Simone Vossel
Combined TMS-fMRI reveals behavior-dependent network effects of right temporoparietal junction neurostimulation in an attentional belief updating task Journal Article
In: Cerebral Cortex, vol. 32, pp. 4698–4714, 2022.
Updating beliefs after unexpected events is fundamental for an optimal adaptation to the environment. Previous findings suggested a causal involvement of the right temporoparietal junction (rTPJ) in belief updating in an attention task. We combined offline continuous theta-burst stimulation (cTBS) over rTPJ with functional magnetic resonance imaging (fMRI) to investigate local and remote stimulation effects within the attention and salience networks. In a sham-controlled, within-subject crossover design, 25 participants performed an attentional cueing task during fMRI with true or false information about cue predictability. By estimating learning rates from response times, we characterized participants' belief updating. Model-derived cue predictability entered the fMRI analysis as a parametric regressor to identify the neural correlates of updating. rTPJ-cTBS effects showed high interindividual variability. The expected learning rate reduction with false cue predictability information by cTBS was only observed in participants showing higher updating in false than in true blocks after sham. cTBS modulated the neural signatures of belief updating, both in rTPJ and in nodes of the attention and salience networks. The interindividual variability of the behavioral cTBS effect was related to differential activity and rTPJ connectivity of the right anterior insula. These results demonstrate a crucial interaction between ventral attention and salience networks for belief updating.
Camille Métais; Judith Nicolas; Moussa Diarra; Alexis Cheviet; Eric Koun; Denis Pélisson
Neural substrates of saccadic adaptation: Plastic changes versus error processing and forward versus backward learning Journal Article
In: NeuroImage, vol. 262, pp. 1–15, 2022.
Previous behavioral, clinical, and neuroimaging studies suggest that the neural substrates of adaptation of saccadic eye movements involve, beyond the central role of the cerebellum, several, still incompletely determined, cortical areas. Furthermore, no neuroimaging study has yet tackled the differences between saccade lengthening ("forward adaptation") and shortening ("backward adaptation") and neither between their two main components, i.e. error processing and oculomotor changes. The present fMRI study was designed to fill these gaps. Blood-oxygen-level-dependent (BOLD) signal and eye movements of 24 healthy volunteers were acquired while performing reactive saccades under 4 conditions repeated in short blocks of 16 trials: systematic target jump during the saccade and in the saccade direction (forward: FW) or in the opposite direction (backward: BW), randomly directed FW or BW target jump during the saccade (random: RND) and no intra-saccadic target jump (stationary: STA). BOLD signals were analyzed both through general linear model (GLM) approaches applied at the whole-brain level and through sensitive Multi-Variate Pattern Analyses (MVPA) applied to 34 regions of interest (ROIs) identified from independent 'Saccade Localizer' functional data. Oculomotor data were consistent with successful induction of forward and backward adaptation in FW and BW blocks, respectively. The different analyses of voxel activation patterns (MVPAs) disclosed the involvement of 1) a set of ROIs specifically related to adaptation in the right occipital cortex, right and left MT/MST, right FEF and right pallidum; 2) several ROIs specifically involved in error signal processing in the left occipital cortex, left PEF, left precuneus, Medial Cingulate cortex (MCC), left inferior and right superior cerebellum; 3) ROIs specific to the direction of adaptation in the occipital cortex and MT/MST (left and right hemispheres for FW and BW, respectively) and in the pallidum of the right hemisphere (FW). The involvement of the left PEF and of the (left and right) occipital cortex were further supported and qualified by the whole brain GLM analysis: clusters of increased activity were found in PEF for the RND versus STA contrast (related to error processing) and in the left (right) occipital cortex for the FW (BW) versus STA contrasts [related to the FW (BW) direction of error and/or adaptation]. The present study both adds complementary data to the growing literature supporting a role of the cerebral cortex in saccadic adaptation through feedback and feedforward relationships with the cerebellum and provides the basis for improving conceptual frameworks of oculomotor plasticity and of its link with spatial cognition.
Viola Mocz; Maryam Vaziri-pashkam; Marvin Chun; Yaoda Xu
Predicting identity-preserving object transformations in human posterior parietal cortex and convolutional neural networks Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, pp. 2406–2435, 2022.
Previous research shows that, within human occipito- temporal cortex (OTC), we can use a general linear mapping function to link visual object responses across nonidentity feature changes, including Euclidean features (e.g., position and size) and non-Euclidean features (e.g., image statistics and spatial frequency). Although the learned mapping is capable of predicting responses of objects not included in training, these predictions are better for categories included than those not included in training. These findings demonstrate a near-orthogonal representation of object identity and nonidentity features throughout human OTC. Here, we extended these findings to examine the mapping across both Euclidean and non-Euclidean feature changes in human posterior parietal cortex (PPC), including functionally defined regions in inferior and superior intraparietal sulcus. We additionally examined responses in five convolutional neural networks (CNNs) pretrained with object classification, as CNNs are considered as the current best model of the primate ventral visual system. We separately compared results from PPC and CNNs with those of OTC. We found that a linear mapping function could successfully link object responses in different states of nonidentity transformations in human PPC and CNNs for both Euclidean and non-Euclidean features. Over-all, we found that object identity and nonidentity features are represented in a near-orthogonal, rather than complete-orthogonal, manner in PPC and CNNs, just like they do in OTC. Meanwhile, some differences existed among OTC, PPC, and CNNs. These results demonstrate the similarities and differences in how visual object information across an identity-preserving image transformation may be represented in OTC, PPC, and CNNs
Robert M. Mok; Bradley C. Love
Abstract neural representations of category membership beyond information coding stimulus or response Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, no. 10, pp. 1719–1735, 2022.
For decades, researchers have debated whether mental representations are symbolic or grounded in sensory inputs and motor programs. Certainly, aspects of mental representations are grounded. However, does the brain also contain abstract concept representations that mediate between perception and action in a flexible manner not tied to the details of sensory inputs and motor programs? Such conceptual pointers would be useful when concepts remain constant despite changes in appearance and associated actions. We evaluated whether human participants acquire such representations using fMRI. Participants completed a probabilistic concept learning task in which sensory, motor, and category variables were not perfectly coupled or entirely independent, making it possible to observe evidence for abstract representations or purely grounded representations. To assess how the learned concept structure is represented in the brain, we examined brain regions implicated in flexible cognition (e.g., pFC and parietal cortex) that are most likely to encode an abstract representation removed from sensory–motor details. We also examined sensory–motor regions that might encode grounded sensory–motor-based representations tuned for categorization. Using a cognitive model to estimate participants' category rule and multivariate pattern analysis of fMRI data, we found the left pFC and human middle temporal visual area (MT)/V5 coded for category in the absence of information coding for stimulus or response. Because category was based on the stimulus, finding an abstract representation of category was not inevitable. Our results suggest that certain brain areas support categorization behavior by constructing concept representations in a format akin to a symbol that differs from stimulus–motor codes.
Roy Moyal; Hamid B. Turker; Wen Ming Luh; Khena M. Swallow
Auditory target detection enhances visual processing and hippocampal functional connectivity Journal Article
In: Frontiers in Psychology, vol. 13, pp. 1–18, 2022.
Though dividing one's attention between two input streams typically impairs performance, detecting a behaviorally relevant stimulus can sometimes enhance the encoding of unrelated information presented at the same time. Previous research has shown that selection of this kind boosts visual cortical activity and memory for concurrent items. An important unanswered question is whether such effects are reflected in processing quality and functional connectivity in visual regions and in the hippocampus. In this fMRI study, participants were asked to memorize a stream of naturalistic images and press a button only when they heard a predefined target tone (400 or 1,200 Hz, counterbalanced). Images could be presented with a target tone, with a distractor tone, or without a tone. Auditory target detection increased activity throughout the ventral visual cortex but lowered it in the hippocampus. Enhancements in functional connectivity between the ventral visual cortex and the hippocampus were also observed following auditory targets. Multi-voxel pattern classification of image category was more accurate on target tone trials than on distractor and no tone trials in the fusiform gyrus and parahippocampal gyrus. This effect was stronger in visual cortical clusters whose activity was more correlated with the hippocampus on target tone than on distractor tone trials. In agreement with accounts suggesting that subcortical noradrenergic influences play a role in the attentional boost effect, auditory target detection also caused an increase in locus coeruleus activity and phasic pupil responses. These findings outline a network of cortical and subcortical regions that are involved in the selection and processing of information presented at behaviorally relevant moments.
Mirjam C. M. Wever; Lisanne A. E. M. Houtum; Loes H. C. Janssen; Wilma G. M. Wentholt; Iris M. Spruit; Marieke S. Tollenaar; Geert Jan Will; Bernet M. Elzinga
Neural and affective responses to prolonged eye contact with one's own adolescent child and unfamiliar others Journal Article
In: NeuroImage, vol. 260, pp. 1–12, 2022.
Eye contact is crucial for the formation and maintenance of social relationships, and plays a key role in facilitating a strong parent-child bond. However, the precise neural and affective mechanisms through which eye contact impacts on parent-child relationships remain elusive. We introduce a task to assess parents' neural and affective responses to prolonged direct and averted gaze coming from their own child, and an unfamiliar child and adult. While in the scanner, 79 parents (n = 44 mothers and n = 35 fathers) were presented with prolonged (16-38 s) videos of their own child, an unfamiliar child, an unfamiliar adult, and themselves (i.e., targets), facing the camera with a direct or an averted gaze. We measured BOLD-responses, tracked parents' eye movements during the videos, and asked them to report on their mood and feelings of connectedness with the targets after each video. Parents reported improved mood and increased feelings of connectedness after prolonged exposure to direct versus averted gaze and these effects were amplified for unfamiliar targets compared to their own child, due to high affect and connectedness ratings after videos of their own child. Neuroimaging results showed that the sight of one's own child was associated with increased activity in middle occipital gyrus, fusiform gyrus and inferior frontal gyrus relative to seeing an unfamiliar child or adult. While we found no robust evidence of specific neural correlates of eye contact (i.e., contrast direct > averted gaze), an exploratory parametric analysis showed that dorsomedial prefrontal cortex (dmPFC) activity increased linearly with duration of eye contact (collapsed across all “other” targets). Eye contact-related dmPFC activity correlated positively with increases in feelings of connectedness, suggesting that this region may drive feelings of connectedness during prolonged eye contact with others. These results underline the importance of prolonged eye contact for affiliative processes and provide first insights into its neural correlates. This may pave the way for new research in individuals or pairs in whom affiliative processes are disrupted.
Antonius Wiehler; Francesca Branzoli; Isaac Adanyeguh; Fanny Mochel; Mathias Pessiglione
A neuro-metabolic account of why daylong cognitive work alters the control of economic decisions Journal Article
In: Current Biology, vol. 32, no. 16, pp. 3564–3575, 2022.
Behavioral activities that require control over automatic routines typically feel effortful and result in cognitive fatigue. Beyond subjective report, cognitive fatigue has been conceived as an inflated cost of cognitive control, objectified by more impulsive decisions. However, the origins of such control cost inflation with cognitive work are heavily debated. Here, we suggest a neuro-metabolic account: the cost would relate to the necessity of recycling potentially toxic substances accumulated during cognitive control exertion. We validated this account using magnetic resonance spectroscopy (MRS) to monitor brain metabolites throughout an approximate workday, during which two groups of participants performed either high-demand or low-demand cognitive control tasks, interleaved with economic decisions. Choice-related fatigue markers were only present in the high-demand group, with a reduction of pupil dilation during decision-making and a preference shift toward short-delay and little-effort options (a low-cost bias captured using computational modeling). At the end of the day, high-demand cognitive work resulted in higher glutamate concentration and glutamate/glutamine diffusion in a cognitive control brain region (lateral prefrontal cortex [lPFC]), relative to low-demand cognitive work and to a reference brain region (primary visual cortex [V1]). Taken together with previous fMRI data, these results support a neuro-metabolic model in which glutamate accumulation triggers a regulation mechanism that makes lPFC activation more costly, explaining why cognitive control is harder to mobilize after a strenuous workday.
Marilena Wilding; Christof Körner; Anja Ischebeck; Natalia Zaretskaya
Increased insula activity precedes the formation of subjective illusory Gestalt Journal Article
In: NeuroImage, vol. 257, pp. 1–10, 2022.
The constructive nature of human perception sometimes leads us to perceiving rather complex impressions from simple sensory input: for example, recognizing animal contours in cloud formations or seeing living creatures in shadows of objects. A special type of bistable stimuli gives us a rare opportunity to study the neural mechanisms behind this process. Such stimuli can be visually interpreted either as simple or as more complex illusory content on the basis of the same sensory input. Previous studies demonstrated increased activity in the superior parietal cortex during the perception of an illusory Gestalt impression compared to a simpler interpretation. Here, we examined the role of slow fluctuations of resting-state fMRI activity in shaping the subsequent illusory interpretation by investigating activity related to the illusory Gestalt not only during, but also prior to its perception. We presented 31 participants with a bistable motion stimulus, which can be perceived either as four moving dot pairs (local) or two moving illusory squares (global). fMRI was used to measure brain activity in a slow event-related design. We observed stronger IPS and putamen responses to the stimulus when participants perceived the global interpretation compared to the local, confirming the findings of previous studies. Most importantly, we also observed that the global stimulus interpretation was preceded by an increased activity of the bilateral dorsal insula, which is known to process saliency and gate information for conscious access. Our data suggest an important role of the dorsal insula in shaping complex illusory interpretations of the sensory input.
Aspen H. Yoo; Alfredo Bolaños; Grace E. Hallenbeck; Masih Rahmati; Thomas C. Sprague; Clayton E. Curtis
Behavioral prioritization enhances working memory precision and neural population gain Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, no. 2, pp. 365–379, 2022.
Humans allocate visual working memory (WM) resource according to behavioral relevance, resulting in more precise memories for more important items. Theoretically, items may be maintained by feature-tuned neural populations, where the relative gain of the populations encoding each item determines precision. To test this hypothesis, we compared the amplitudes of delay period activity in the different parts of retinotopic maps representing each of several WM items, predicting the amplitudes would track behavioral priority. Using fMRI, we scanned participants while they remembered the location of multiple items over a WM delay and then reported the location of one probed item using a memory-guided saccade. Importantly, items were not equally probable to be probed (0.6, 0.3, 0.1, 0.0), which was indicated with a precue. We analyzed fMRI activity in 10 visual field maps in occipital, parietal, and frontal cortex known to be important for visual WM. In early visual cortex, but not association cortex, the amplitude of BOLD activation within voxels corresponding to the retinotopic location of visual WM items increased with the priority of the item. Interestingly, these results were contrasted with a common finding that higher-level brain regions had greater delay period activity, demonstrating a dissociation between the absolute amount of activity in a brain area and the activity of different spatially selective populations within it. These results suggest that the distribution of WM resources according to priority sculpts the relative gains of neural populations that encode items, offering a neural mechanism for how prioritization impacts memory precision.
Farnaz Zamani Esfahlani; Lisa Byrge; Jacob Tanner; Olaf Sporns; Daniel P. Kennedy; Richard F. Betzel
Edge-centric analysis of time-varying functional brain networks with applications in autism spectrum disorder Journal Article
In: NeuroImage, vol. 263, pp. 1–12, 2022.
The interaction between brain regions changes over time, which can be characterized using time-varying functional connectivity (tvFC). The common approach to estimate tvFC uses sliding windows and offers limited temporal resolution. An alternative method is to use the recently proposed edge-centric approach, which enables the tracking of moment-to-moment changes in co-fluctuation patterns between pairs of brain regions. Here, we first examined the dynamic features of edge time series and compared them to those in the sliding window tvFC (sw-tvFC). Then, we used edge time series to compare subjects with autism spectrum disorder (ASD) and healthy controls (CN). Our results indicate that relative to sw-tvFC, edge time series captured rapid and bursty network-level fluctuations that synchronize across subjects during movie-watching. The results from the second part of the study suggested that the magnitude of peak amplitude in the collective co-fluctuations of brain regions (estimated as root sum square (RSS) of edge time series) is similar in CN and ASD. However, the trough-to-trough duration in RSS signal is greater in ASD, compared to CN. Furthermore, an edge-wise comparison of high-amplitude co-fluctuations showed that the within-network edges exhibited greater magnitude fluctuations in CN. Our findings suggest that high-amplitude co-fluctuations captured by edge time series provide details about the disruption of functional brain dynamics that could potentially be used in developing new biomarkers of mental disorders.
Bo Zhang; Yuji Naya
A dataset of human fMRI/MEG experiments with eye tracking for spatial memory research using virtual reality Journal Article
In: Data in Brief, vol. 43, pp. 1–8, 2022.
A dataset consisting of whole-brain fMRI (functional magnetic resonance imaging)/MEG (magnetoencephalography) images, eye tracking files, and behavioral records from healthy adult human participants when they performed a spatial-memory paradigm in a virtual environment was collected to investigate the neural representation of the cognitive map defined by unique spatial relationship of three objects, as well as the neural dynamics of the cognitive map following the task demand from localizing self-location to remembering the target location relative to the self-body. The dataset, including both fMRI and MEG, was also used to investigate the neural networks involved in representing a target within and outside the visual field. The dataset included 19 and 12 university students at Peking University for fMRI and MEG experiments, respectively (fMRI: 12 women, 7 men; MEG: 4 women, 8 men). The average ages of those participants were 24.9 years (MRI: 18–30 years) and 22.5 years (MEG: 19–25 years), respectively. fMRI BOLD and T1-weighted images were acquired using a 3T Siemens Prisma scanner (Siemens, Erlangen, Germany) equipped with a 20-channel receiver head coil. MEG neuromagnetic data were acquired using a 275-channel MEG system (CTF MEG, Canada). The dataset could be further used to investigate a range of neural mechanisms involved in human spatial cognition or to develop a bioinspired deep neural network to enhance machines' abilities in spatial processing.
Ying Zhou; Clayton E. Curtis; Kartik K. Sreenivasan; Daryl Fougnie
Common neural mechanisms control attention and working memory Journal Article
In: Journal of Neuroscience, vol. 42, no. 37, pp. 7110–7120, 2022.
Although previous studies point to qualitative similarities between working memory (WM) and attention, the degree to which these two constructs rely on shared neural mechanisms remains unknown. Focusing on one such potentially shared mechanism, we tested the hypothesis that selecting an item within WM utilizes similar neural mechanisms as selecting a visible item via a shift of attention. We used fMRI and machine learning to decode both the selection among items visually available and the selection among items stored in WM in human subjects (both sexes). Patterns of activity in visual, parietal, and to a lesser extent frontal cortex predicted the locations of the selected items. Critically, these patterns were strikingly interchangeable; classifiers trained on data during attentional selection predicted selection from WM, and classifiers trained on data during selection from memory predicted attentional selection. Using models of voxel receptive fields, we visualized topographic population activity that revealed gain enhancements at the locations of the externally and internally selected items. Our results suggest that selecting among perceived items and selecting among items in WM share a common mechanism. This common mechanism, analogous to a shift of spatial attention, controls the relative gains of neural populations that encode behaviorally relevant information.
Erin Goddard; Thomas A. Carlson; Alexandra Woolgar
Spatial and feature-selective attention have distinct, interacting effects on population-level tuning Journal Article
In: Journal of Cognitive Neuroscience, vol. 34, no. 2, pp. 290–312, 2022.
Attention can be deployed in different ways: When searching for a taxi in New York City, we can decide where to attend (e.g., to the street) and what to attend to (e.g., yellow cars). Although we use the same word to describe both processes, nonhuman primate data suggest that these produce distinct effects on neural tuning. This has been challenging to assess in humans, but here we used an opportunity afforded by multivariate decoding of MEG data. We found that attending to an object at a particular location and attending to a particular object feature produced effects that interacted multiplicatively. The two types of attention induced distinct patterns of enhancement in occipital cortex, with feature-selective attention producing relatively more enhancement of small feature differences and spatial attention producing relatively larger effects for larger feature differences. An information flow analysis further showed that stimulus representations in occipital cortex were Granger-caused by coding in frontal cortices earlier in time and that the timing of this feedback matched the onset of attention effects. The data suggest that spatial and feature-selective attention rely on distinct neural mechanisms that arise from frontal-occipital information exchange, interacting multiplicatively to selectively enhance task-relevant information.
Timo L. Kvamme; Mesud Sarmanlu; Christopher Bailey; Morten Overgaard
Neurofeedback modulation of the sound-induced flash illusion using parietal cortex alpha oscillations reveals dependency on prior multisensory congruency Journal Article
In: Neuroscience, vol. 482, pp. 1–17, 2022.
Spontaneous neural oscillations are key predictors of perceptual decisions to bind multisensory sig- nals into a unified percept. Research links decreased alpha power in the posterior cortices to attention and audio- visual binding in the sound-induced flash illusion (SIFI) paradigm. This suggests that controlling alpha oscillations would be a way of controlling audiovisual binding. In the present feasibility study we used MEG- neurofeedback to train one group of subjects to increase left/right and another to increase right/left alpha power ratios in the parietal cortex. We tested for changes in audiovisual binding in a SIFI paradigm where flashes appeared in both hemifields. Results showed that the neurofeedback induced a significant asymmetry in alpha power for the left/right group, not seen for the right/left group. Corresponding asymmetry changes in audiovisual binding in illusion trials (with 2, 3, and 4 beeps paired with 1 flash) were not apparent. Exploratory analyses showed that neurofeedback training effects were present for illusion trials with the lowest numeric disparity (i.e., 2 beeps and 1 flash trials) only if the previous trial had high congruency (2 beeps and 2 flashes). Our data suggest that the relation between parietal alpha power (an index of attention) and its effect on audiovisual binding is dependent on the learned causal structure in the previous stimulus. The present results suggests that low alpha power biases observers towards audiovisual binding when they have learned that audiovisual signals orig- inate from a common origin, consistent with a Bayesian causal inference account of multisensory perception.
Emily J. Allen; Ghislain St-Yves; Yihan Wu; Jesse L. Breedlove; Jacob S. Prince; Logan T. Dowdle; Matthias Nau; Brad Caron; Franco Pestilli; Ian Charest; J. Benjamin Hutchinson; Thomas Naselaris; Kendrick Kay
A massive 7T fMRI dataset to bridge cognitive neuroscience and artificial intelligence Journal Article
In: Nature Neuroscience, vol. 25, no. 1, pp. 116–126, 2022.
Extensive sampling of neural activity during rich cognitive phenomena is critical for robust understanding of brain function. Here we present the Natural Scenes Dataset (NSD), in which high-resolution functional magnetic resonance imaging responses to tens of thousands of richly annotated natural scenes were measured while participants performed a continuous recognition task. To optimize data quality, we developed and applied novel estimation and denoising techniques. Simple visual inspections of the NSD data reveal clear representational transformations along the ventral visual pathway. Further exemplifying the inferential power of the dataset, we used NSD to build and train deep neural network models that predict brain activity more accurately than state-of-the-art models from computer vision. NSD also includes substantial resting-state and diffusion data, enabling network neuroscience perspectives to constrain and enhance models of perception and memory. Given its unprecedented scale, quality and breadth, NSD opens new avenues of inquiry in cognitive neuroscience and artificial intelligence.
Bertrand Beffara; Fadila Hadj-Bouziane; Suliann Ben Hamed; C. Nico Boehler; Leonardo Chelazzi; Elisa Santandrea; Emiliano Macaluso
Dynamic causal interactions between occipital and parietal cortex explain how endogenous spatial attention and stimulus-driven salience jointly shape the distribution of processing priorities in 2D visual space Journal Article
In: NeuroImage, vol. 255, pp. 1–18, 2022.
Visuo-spatial attention prioritizes the processing of relevant inputs via different types of signals, including current goals and stimulus salience. Complex mixtures of these signals engage in everyday life situations, but little is known about how these signals jointly modulate distributed patterns of activity across the occipital regions that represent visual space. Here, we measured spatio-topic, quadrant-specific occipital activity during the processing of visual displays containing both task-relevant targets and salient color-singletons. We computed spatial bias vectors indexing the effect of attention in 2D space, as coded by distributed activity in the occipital cortex. We found that goal-directed spatial attention biased activity towards the target and that salience further modulated this endogenous effect: salient distractors decreased the spatial bias, while salient targets increased it. Analyses of effective connectivity revealed that the processing of salient distractors relied on the modulation of the bidirectional connectivity between the occipital and the posterior parietal cortex, as well as the modulation of the lateral interactions within the occipital cortex. These findings demonstrate that goal-directed attention and salience jointly contribute to shaping processing priorities in the occipital cortex and highlight that multiple functional paths determine how spatial information about these signals is distributed across occipital regions.
Daniel K. Bjornn; Julie Van; C. Brock Kirwan
The contributions of eye gaze fixations and target-lure similarity to behavioral and fMRI indices of pattern separation and pattern completion Journal Article
In: Cognitive Neuroscience, vol. 13, no. 3-4, pp. 171–181, 2022.
Pattern separation and pattern completion are generally studied in humans using mnemonic discrimination tasks such as the Mnemonic Similarity Task (MST) where participants identify similar lures and repeated items from a series of images. Failures to correctly discriminate lures are thought to reflect a failure of pattern separation and a propensity toward pattern completion. Recent research has challenged this perspective, suggesting that poor encoding rather than pattern completion accounts for the occurrence of false alarm responses to similar lures. In two experiments, participants completed a continuous recognition task version of the MST while eye movement (Experiments 1 and 2) and fMRI data (Experiment 2) were collected. In Experiment 1, we replicated the result that fixation counts at study predicted accuracy on lure trials (consistent with poor encoding predicting mnemonic discrimination performance), but this effect was not observed in our fMRI task. In both experiments, we found that target-lure similarity was a strong predictor of accuracy on lure trials. Further, we found that fMRI activation changes in the hippocampus were significantly correlated with the number of fixations at study for correct but not incorrect mnemonic discrimination judgments when controlling for target-lure similarity. Our findings indicate that while eye movements during encoding predict subsequent hippocampal activation changes for correct mnemonic discriminations, the predictive power of eye movements for activation changes for incorrect mnemonic discrimination trials was modest at best.
Charlie S. Burlingham; Minyoung Ryoo; Zvi N. Roth; Saghar Mirbagheri; David J. Heeger; Elisha P. Merriam
Task-related hemodynamic responses in human early visual cortex are modulated by task difficulty and behavioral performance Journal Article
In: eLife, vol. 11, pp. 1–24, 2022.
Early visual cortex exhibits widespread hemodynamic responses in the absence of visual stimulation, which are entrained to the timing of a task and not predicted by local spiking or local field potential. Such task-related responses (TRRs) covary with reward magnitude and physiological signatures of arousal. It is unknown, however, if TRRs change on a trial-to-trial basis according to behavioral performance and task difficulty. If so, this would suggest that TRRs reflect arousal on a trial-to-trial timescale and covary with critical task and behavioral variables. We measured functional magnetic resonance imaging blood-oxygen-level-dependent (fMRI-BOLD) responses in the early visual cortex of human observers performing an orientation discrimination task consisting of separate easy and hard runs of trials. Stimuli were presented in a small portion of one hemifield, but the fMRI response was measured in the ipsilateral hemisphere, far from the stimulus representation and focus of spatial attention. TRRs scaled in amplitude with task difficulty, behavioral accuracy, reaction time, and lapses across trials. These modulations were not explained by the influence of respiration, cardiac activity, or head movement on the fMRI signal. Similar modulations with task difficulty and behavior were observed in pupil size. These results suggest that TRRs reflect arousal and behavior on the timescale of individual trials.
Lisa Byrge; Dorit Kliemann; Ye He; Hu Cheng; Julian Michael Tyszka; Ralph Adolphs; Daniel P. Kennedy
Video-evoked fMRI BOLD responses are highly consistent across different data acquisition sites Journal Article
In: Human Brain Mapping, vol. 43, no. 9, pp. 2972–2991, 2022.
Naturalistic imaging paradigms, in which participants view complex videos in the scanner, are increasingly used in human cognitive neuroscience. Videos evoke temporally synchronized brain responses that are similar across subjects as well as within subjects, but the reproducibility of these brain responses across different data acquisition sites has not yet been quantified. Here, we characterize the consistency of brain responses across independent samples of participants viewing the same videos in functional magnetic resonance imaging (fMRI) scanners at different sites (Indiana University and Caltech). We compared brain responses collected at these different sites for two carefully matched datasets with identical scanner models, acquisition, and preprocessing details, along with a third unmatched dataset in which these details varied. Our overall conclusion is that for matched and unmatched datasets alike, video-evoked brain responses have high consistency across these different sites, both when compared across groups and across pairs of individuals. As one might expect, differences between sites were larger for unmatched datasets than matched datasets. Residual differences between datasets could in part reflect participant-level variability rather than scanner- or data- related effects. Altogether our results indicate promise for the development and, critically, generalization of video fMRI studies of individual differences in healthy and clinical populations alike.
Youngsun T. Cho; Flora Moujaes; Charles H. Schleifer; Martina Starc; Jie Lisa Ji; Nicole Santamauro; Brendan Adkinson; Antonija Kolobaric; Morgan Flynn; John H. Krystal; John D. Murray; Grega Repovs; Alan Anticevic
Reward and loss incentives improve spatial working memory by shaping trial-by-trial posterior frontoparietal signals Journal Article
In: NeuroImage, vol. 254, pp. 1–15, 2022.
Integrating motivational signals with cognition is critical for goal-directed activities. The mechanisms that link neural changes with motivated working memory continue to be understood. Here, we tested how externally cued and non-cued (internally represented) reward and loss impact spatial working memory precision and neural circuits in human subjects using fMRI. We translated the classic delayed-response spatial working memory paradigm from non-human primate studies to take advantage of a continuous numeric measure of working memory precision, and the wealth of translational neuroscience yielded by these studies. Our results demonstrated that both cued and non-cued reward and loss improved spatial working memory precision. Visual association regions of the posterior prefrontal and parietal cortices, specifically the precentral sulcus (PCS) and intraparietal sulcus (IPS), had increased BOLD signal during incentivized spatial working memory. A subset of these regions had trial-by-trial increases in BOLD signal that were associated with better working memory precision, suggesting that these regions may be critical for linking neural signals with motivated working memory. In contrast, regions straddling executive networks, including areas in the dorsolateral prefrontal cortex, anterior parietal cortex and cerebellum displayed decreased BOLD signal during incentivized working memory. While reward and loss similarly impacted working memory processes, they dissociated during feedback when money won or avoided in loss was given based on working memory performance. During feedback, the trial-by-trial amount and valence of reward/loss received was dissociated amongst regions such as the ventral striatum, habenula and periaqueductal gray. Overall, this work suggests motivated spatial working memory is supported by complex sensory processes, and that the IPS and PCS in the posterior frontoparietal cortices may be key regions for integrating motivational signals with spatial working memory precision.
Nicolas Clairis; Mathias Pessiglione
Value, confidence, deliberation: A functional partition of the medial prefrontal cortex demonstrated across rating and choice tasks Journal Article
In: Journal of Neuroscience, vol. 42, no. 28, pp. 1–41, 2022.
Deciding about courses of action involves minimizing costs and maximizing benefits. Decision neuroscience studies have implicated both the ventral and dorsal medial PFC (vmPFC and dmPFC) in signaling goal value and action cost, but the precise functional role of these regions is still a matter of debate. Here, we suggest a more general functional partition that applies not only to decisions but also to judgments about goal value (expected reward) and action cost (expected effort). In this conceptual framework, cognitive representations related to options (reward value and effort cost) are dissociated from metacognitive representations (confidence and deliberation) related to solving the task (providing a judgment or making a choice). We used an original approach aimed at identifying consistencies across several preference tasks, from likeability ratings to binary decisions involving both attribute integration and option comparison. fMRI results in human male and female participants confirmed the vmPFC as a generic valuation system, its activity increasing with reward value and decreasing with effort cost. In contrast, more dorsal regions were not concerned with the valuation of options but with metacognitive variables, confidence being reflected in mPFC activity and deliberation time in dmPFC activity. Thus, there was a dissociation between the effort attached to choice options (represented in the vmPFC) and the effort invested in deliberation (represented in the dmPFC), the latter being expressed in pupil dilation. More generally, assessing commonalities across preference tasks might help in reaching a unified view of the neural mechanisms underlying the cost/benefit tradeoffs that drive human behavior.
Xiaohui Cui; Fabio Richlan; Wei Zhou
Fixation-related fMRI analysis reveals the neural basis of parafoveal processing in self-paced reading of Chinese words Journal Article
In: Brain Structure and Function, vol. 227, no. 8, pp. 2609–2621, 2022.
While parafoveal word processing plays an important role in natural reading, the underlying neural mechanism remains unclear. The present study investigated the neural basis of parafoveal processing during Chinese word reading with the co-registration of eye-tracking and functional magnetic resonance imaging (fMRI) using fixation-related fMRI analysis. In the gaze-contingent boundary paradigm, preview conditions (words that are identical, orthographically similar, and unrelated to target words), pre-target word frequency and target word frequency were manipulated. When fixating the pre-target word, the identical preview condition elicited lower brain activation in the left fusiform gyrus relative to unrelated and orthographically similar preview conditions and there were significant interactions of preview condition and pre-target word frequency on brain activation of the left middle frontal gyrus, left fusiform gyrus and supplementary motor area. When fixating the target word, there was a significant main effect of preview condition on brain activation of the right fusiform gyrus and a significant interaction of preview condition and pre-target word frequency on brain activation of the left middle frontal gyrus. These results suggest that fixation-related brain activation provides immediate measures and new perspectives to understand the mechanism of parafoveal processing in self-paced reading.
Jasper H. Fabius; Katarina Moravkova; Alessio Fracasso
Topographic organization of eye-position dependent gain fields in human visual cortex Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–16, 2022.
The ability to move has introduced animals with the problem of sensory ambiguity: the position of an external stimulus could change over time because the stimulus moved, or because the animal moved its receptors. This ambiguity can be resolved with a change in neural response gain as a function of receptor orientation. Here, we developed an encoding model to capture gain modulation of visual responses in high field (7 T) fMRI data. We characterized population eye-position dependent gain fields (pEGF). The information contained in the pEGFs allowed us to reconstruct eye positions over time across the visual hierarchy. We discovered a systematic distribution of pEGF centers: pEGF centers shift from contra- to ipsilateral following pRF eccentricity. Such a topographical organization suggests that signals beyond pure retinotopy are accessible early in the visual hierarchy, providing the potential to solve sensory ambiguity and optimize sensory processing information for functionally relevant behavior.
Farzad V. Farahani; Waldemar Karwowski; Mark D'Esposito; Richard F. Betzel; Pamela K. Douglas; Anna Maria Sobczak; Bartosz Bohaterewicz; Tadeusz Marek; Magdalena Fafrowicz
Diurnal variations of resting-state fMRI data: A graph-based analysis Journal Article
In: NeuroImage, vol. 256, pp. 1–25, 2022.
Circadian rhythms (lasting approximately 24 h) control and entrain various physiological processes, ranging from neural activity and hormone secretion to sleep cycles and eating habits. Several studies have shown that time of day (TOD) is associated with human cognition and brain functions. In this study, utilizing a chronotype-based paradigm, we applied a graph theory approach on resting-state functional MRI (rs-fMRI) data to compare whole-brain functional network topology between morning and evening sessions and between morning-type (MT) and evening-type (ET) participants. Sixty-two individuals (31 MT and 31 ET) underwent two fMRI sessions, approximately 1 hour (morning) and 10 h (evening) after their wake-up time, according to their declared habitual sleep-wake pattern on a regular working day. In the global analysis, the findings revealed the effect of TOD on functional connectivity (FC) patterns, including increased small-worldness, assortativity, and synchronization across the day. However, we identified no significant differences based on chronotype categories. The study of the modular structure of the brain at mesoscale showed that functional networks tended to be more integrated with one another in the evening session than in the morning session. Local/regional changes were affected by both factors (i.e., TOD and chronotype), mostly in areas associated with somatomotor, attention, frontoparietal, and default networks. Furthermore, connectivity and hub analyses revealed that the somatomotor, ventral attention, and visual networks covered the most highly connected areas in the morning and evening sessions: the latter two were more active in the morning sessions, and the first was identified as being more active in the evening. Finally, we performed a correlation analysis to determine whether global and nodal measures were associated with subjective assessments across participants. Collectively, these findings contribute to an increased understanding of diurnal fluctuations in resting brain activity and highlight the role of TOD in future studies on brain function and the design of fMRI experiments.
Mahtab Farahbakhsh; Elaine J. Anderson; Roni O. Maimon-Mor; Andy Rider; John A. Greenwood; Nashila Hirji; Serena Zaman; Pete R. Jones; D. Samuel Schwarzkopf; Geraint Rees; Michel Michaelides; Tessa M. Dekker
A demonstration of cone function plasticity after gene therapy in achromatopsia Journal Article
In: Brain, vol. 145, pp. 3803–3815, 2022.
Recent advances in regenerative therapy have placed the treatment of previously incurable eye diseases within arms' reach. Achromatopsia is a severe monogenic heritable retinal disease that disrupts cone function from birth, leaving patients with complete colour blindness, low acuity, photosensitivity and nystagmus. While successful gene-replacement therapy in non-primate models of achromatopsia has raised widespread hopes for clinical treatment, it was yet to be determined if and how these therapies can induce new cone function in the human brain. Using a novel multimodal approach, we demonstrate for the first time that gene therapy can successfully activate dormant cone-mediated pathways in children with achromatopsia (CNGA3- and CNGB3-associated, 10–15 years). To test this, we combined functional MRI population receptive field mapping and psychophysics with stimuli that selectively measure cone photoreceptor signalling. We measured cortical and visual cone function before and after gene therapy in four paediatric patients, evaluating treatment-related change against benchmark data from untreated patients (n = 9) and normal-sighted participants (n = 28). After treatment, two of the four children displayed strong evidence for novel cone-mediated signals in visual cortex, with a retinotopic pattern that was not present in untreated achromatopsia and which is highly unlikely to emerge by chance. Importantly, this change was paired with a significant improvement in psychophysical measures of cone-mediated visual function. These improvements were specific to the treated eye, and provide strong evidence for successful read-out and use of new cone-mediated information. These data show for the first time that gene replacement therapy in achromatopsia within the plastic period of development can awaken dormant cone-signalling pathways after years of deprivation. This reveals unprecedented neural plasticity in the developing human nervous system and offers great promise for emerging regenerative therapies.
Julia Fietz; Dorothee Pöhlchen; Florian P. Binder; Michael Czisch; Philipp G. Sämann; Victor I. Spoormaker
Pupillometry tracks cognitive load and salience network activity in a working memory functional magnetic resonance imaging task Journal Article
In: Human Brain Mapping, vol. 43, no. 2, pp. 665–680, 2022.
The diameter of the human pupil tracks working memory processing and is associated with activity in the frontoparietal network. At the same time, recent neuroimaging research has linked human pupil fluctuations to activity in the salience network. In this combined functional magnetic resonance imaging (fMRI)/pupillometry study, we recorded the pupil size of healthy human participants while they performed a blockwise organized working memory task (N-back) inside an MRI scanner in order to monitor the pupil fluctuations associated neural activity during working memory processing. We first confirmed that mean pupil size closely followed working memory load. Combining this with fMRI data, we focused on blood oxygen level dependent (BOLD) correlates of mean pupil size modeled onto the task blocks as a parametric modulation. Interrogating this modulated task regressor, we were able to retrieve the frontoparietal network. Next, to fully exploit the within-block dynamics, we divided the blocks into 1 s time bins and filled these with corresponding pupil change values (first-order derivative of pupil size). We found that pupil change within N-back blocks was positively correlated with BOLD amplitudes in the areas of the salience network (namely bilateral insula, and anterior cingulate cortex). Taken together, fMRI with simultaneous measurement of pupil parameters constitutes a valuable tool to dissect working memory subprocesses related to both working memory load and salience of the presented stimuli.
Joshua J. Foster; Sam Ling
Feature-based attention multiplicatively scales the fMRI-BOLD contrast-response function Journal Article
In: Journal of Neuroscience, vol. 42, no. 36, pp. 6894–6906, 2022.
fMRI plays a key role in the study of attention. However, there remains a puzzling discrepancy between attention effects measured with fMRI and with electrophysiological methods. While electrophysiological studies find that attention increases sensory gain, amplifying stimulus-evoked neural responses by multiplicatively scaling the contrast-response function (CRF), fMRI appears to be insensitive to these multiplicative effects. Instead, fMRI studies typically find that attention produces an additive baseline shift in the BOLD signal. These findings suggest that attentional effects measured with fMRI reflect top-down inputs to visual cortex, rather than the modulation of sensory gain. If true, this drastically limits what fMRI can tell us about how attention improves sensory coding. Here, we examined whether fMRI is sensitive to multiplicative effects of attention using a feature-based attention paradigm designed to preclude any possible additive effects. We measured BOLD activity evoked by a probe stimulus in one visual hemifield while participants (6 male, 6 female) attended to the probe orientation (attended condition), or to an orthogonal orientation (unattended condition), in the other hemifield. To measure CRFs in visual areas V1-V3, we parametrically varied the contrast of the probe stimulus. In all three areas, feature-based attention increased contrast gain, improving sensitivity by shifting CRFs toward lower contrasts. In V2 and V3, we also found an increase in response gain, an increase in the responsivity of the CRF, that was greatest at inner eccentricities. These results provide clear evidence that the fMRI-BOLD signal is sensitive to multiplicative effects of attention.
Mathilda Froesel; Maëva Gacoin; Simon Clavagnier; Marc Hauser; Quentin Goudard; Suliann Ben Hamed
Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain Journal Article
In: Nature Communications, vol. 13, no. 1, pp. 1–17, 2022.
Social interactions rely on the interpretation of semantic and emotional information, often from multiple sensory modalities. Nonhuman primates send and receive auditory and visual communicative signals. However, the neural mechanisms underlying the association of visual and auditory information based on their common social meaning are unknown. Using heart rate estimates and functional neuroimaging, we show that in the lateral and superior temporal sulcus of the macaque monkey, neural responses are enhanced in response to species-specific vocalisations paired with a matching visual context, or when vocalisations follow, in time, visual information, but inhibited when vocalisation are incongruent with the visual context. For example, responses to affiliative vocalisations are enhanced when paired with affiliative contexts but inhibited when paired with aggressive or escape contexts. Overall, we propose that the identified neural network represents social meaning irrespective of sensory modality.
Clément M. Garin; Yuki Hori; Stefan Everling; Christopher T. Whitlow; Finnegan J. Calabro; Beatriz Luna; Mathilda Froesel; Maëva Gacoin; Suliann Ben Hamed; Marc Dhenain; Christos Constantinidis
An evolutionary gap in primate default mode network organization Journal Article
In: Cell Reports, vol. 39, no. 2, pp. 1–17, 2022.
The human default mode network (DMN) is engaged at rest and in cognitive states such as self-directed thoughts. Interconnected homologous cortical areas in primates constitute a network considered as the equivalent. Here, based on a cross-species comparison of the DMN between humans and non-hominoid primates (macaques, marmosets, and mouse lemurs), we report major dissimilarities in connectivity profiles. Most importantly, the medial prefrontal cortex (mPFC) of non-hominoid primates is poorly engaged with the posterior cingulate cortex (PCC), though strong correlated activity between the human PCC and the mPFC is a key feature of the human DMN. Instead, a fronto-temporal resting-state network involving the mPFC was detected consistently across non-hominoid primate species. These common functional features shared between non-hominoid primates but not with humans suggest a substantial gap in the organization of the primate's DMN and its associated cognitive functions.
Laura S. Geurts; James R. H. Cooke; Ruben S. Bergen; Janneke F. M. Jehee
Subjective confidence reflects representation of Bayesian probability in cortex Journal Article
In: Nature Human Behaviour, vol. 6, pp. 294–305, 2022.
What gives rise to the human sense of confidence? Here we tested the Bayesian hypothesis that confidence is based on a probability distribution represented in neural population activity. We implemented several computational models of confidence and tested their predictions using psychophysics and functional magnetic resonance imaging. Using a generative model-based decoding technique, we extracted probability distributions from neural population activity in human visual cortex. We found that subjective confidence tracks the shape of the decoded distribution. That is, when sensory evidence was more precise, as indicated by the decoded distribution, observers reported higher levels of confidence. We furthermore found that neural activity in the insula, anterior cingulate and prefrontal cortex was linked to both the shape of the decoded distribution and reported confidence, in ways consistent with the Bayesian model. Altogether, our findings support recent statistical theories of confidence and suggest that probabilistic information guides the computation of one's sense of confidence.
Camille Giacometti; Audrey Dureux; Delphine Autran-Clavagnier; Charles R. E. Wilson; Jérôme Sallet; Manon Dirheimer; Emmanuel Procyk; Fadila Hadj-Bouziane; Céline Amiez
Frontal cortical functional connectivity is impacted by anaesthesia in macaques Journal Article
In: Cerebral Cortex, vol. 32, pp. 4050–4067, 2022.
A critical aspect of neuroscience is to establish whether and how brain networks evolved across primates. To date, most comparative studies have used resting-state functional magnetic resonance imaging (rs-fMRI) in anaesthetized nonhuman primates and in awake humans. However, anaesthesia strongly affects rs-fMRI signals. The present study investigated the impact of the awareness state (anaesthesia vs. awake) within the same group of macaque monkeys on the rs-fMRI functional connectivity organization of a well-characterized network in the human brain, the cingulo-frontal lateral network. Results in awake macaques show that rostral seeds in the cingulate sulcus exhibited stronger correlation strength with rostral compared to caudal lateral frontal cortical areas, while more caudal seeds displayed stronger correlation strength with caudal compared to anterior lateral frontal cortical areas. Critically, this inverse rostro-caudal functional gradient was abolished under anaesthesia. This study demonstrated a similar functional connectivity (FC) organization of the cingulo-frontal cortical network in awake macaque to that previously uncovered in the human brain pointing toward a preserved FC organization from macaque to human. However, it can only be observed in awake state suggesting that this network is sensitive to anaesthesia and warranting significant caution when comparing FC patterns across species under different states.
Mengyuan Gong; Yilin Chen; Taosheng Liu
Preparatory attention to visual features primarily relies on non-sensory representation Journal Article
In: Scientific Reports, vol. 12, no. 1, pp. 1–12, 2022.
Prior knowledge of behaviorally relevant information promotes preparatory attention before the appearance of stimuli. A key question is how our brain represents the attended information during preparation. A sensory template hypothesis assumes that preparatory signals evoke neural activity patterns that resembled the perception of the attended stimuli, whereas a non-sensory, abstract template hypothesis assumes that preparatory signals reflect the abstraction of attended stimuli. To test these hypotheses, we used fMRI and multivariate analysis to characterize neural activity patterns when human participants were prepared to attend a feature and then select it from a compound stimulus. In an fMRI experiment using basic visual feature (motion direction), we observed reliable decoding of the to-be-attended feature from the preparatory activity in both visual and frontoparietal areas. However, while the neural patterns constructed by a single feature from a baseline task generalized to the activity patterns during stimulus selection, they could not generalize to the activity patterns during preparation. Our findings thus suggest that neural signals during attentional preparation are predominantly non-sensory in nature that may reflect an abstraction of the attended feature. Such a representation could provide efficient and stable guidance of attention.
Mats W. J. Es; Tom R. Marshall; Eelke Spaak; Ole Jensen; Jan-Mathijs Schoffelen
Phasic modulation of visual representations during sustained attention Journal Article
In: European Journal of Neuroscience, vol. 55, no. 11-12, pp. 3191–3208, 2022.
Sustained attention has long been thought to benefit perception in a continuous fashion, but recent evidence suggests that it affects perception in a discrete, rhythmic way. Periodic fluctuations in behavioral performance over time, and modulations of behavioral performance by the phase of spontaneous oscillatory brain activity point to an attentional sampling rate in the theta or alpha frequency range. We investigated whether such discrete sampling by attention is reflected in periodic fluctuations in the decodability of visual stimulus orientation from magnetoencephalographic (MEG) brain signals. In this exploratory study, human subjects attended one of the two grating stimuli, while MEG was being recorded. We assessed the strength of the visual representation of the attended stimulus using a support vector machine (SVM) to decode the orientation of the grating (clockwise vs. counterclockwise) from the MEG signal. We tested whether decoder performance depended on the theta/alpha phase of local brain activity. While the phase of ongoing activity in the visual cortex did not modulate decoding performance, theta/alpha phase of activity in the frontal eye fields and parietal cortex, contralateral to the attended stimulus did modulate decoding performance. These findings suggest that phasic modulations of visual stimulus representations in the brain are caused by frequency-specific top-down activity in the frontoparietal attention network, though the behavioral relevance of these effects could not be established.
Laura Müller-Pinzler; Nora Czekalla; Annalina V. Mayer; Alexander Schröder; David S. Stolz; Frieder M. Paulus; Sören Krach
Neurocomputational mechanisms of affected beliefs Journal Article
In: Communications Biology, vol. 5, no. 1, pp. 1–16, 2022.
The feedback people receive on their behavior shapes the process of belief formation and self-efficacy in mastering a particular task. However, the neural and computational mechanisms of how the subjective value of self-efficacy beliefs, and the corresponding affect, influence the learning process remain unclear. We investigated these mechanisms during self-efficacy belief formation using fMRI, pupillometry, and computational modeling, and by analyzing individual differences in affective experience. Biases in the formation of self-efficacy beliefs were associated with affect, pupil dilation, and neural activity within the anterior insula, amygdala, ventral tegmental area/ substantia nigra, and mPFC. Specifically, neural and pupil responses mapped the valence of the prediction errors in correspondence with individuals' experienced affective states and learning biases during self-efficacy belief formation. Together with the functional connectivity dynamics of the anterior insula within this network, our results provide evidence for neural and computational mechanisms of how we arrive at affected beliefs.
Abigail L. Noyce; Ray W. Lefco; James A. Brissenden; Sean M. Tobyne; Barbara G. Shinn-Cunningham; David C. Somers
Extended frontal networks for visual and auditory working memory Journal Article
In: Cerebral Cortex, vol. 32, pp. 855–869, 2022.
Working memory (WM) supports the persistent representation of transient sensory information. Visual and auditory stimuli place different demands on WM and recruit different brain networks. Separate auditory- and visual-biased WM networks extend into the frontal lobes, but several challenges confront attempts to parcellate human frontal cortex, including fine-grained organization and between-subject variability. Here, we use differential intrinsic functional connectivity from 2 visual-biased and 2 auditory-biased frontal structures to identify additional candidate sensory-biased regions in frontal cortex. We then examine direct contrasts of task functional magnetic resonance imaging during visual versus auditory 2-back WM to validate those candidate regions. Three visual-biased and 5 auditory-biased regions are robustly activated bilaterally in the frontal lobes of individual subjects (N = 14, 7 women). These regions exhibit a sensory preference during passive exposure to task stimuli, and that preference is stronger during WM. Hierarchical clustering analysis of intrinsic connectivity among novel and previously identified bilateral sensory-biased regions confirms that they functionally segregate into visual and auditory networks, even though the networks are anatomically interdigitated. We also observe that the frontotemporal auditory WM network is highly selective and exhibits strong functional connectivity to structures serving non-WM functions, while the frontoparietal visual WM network hierarchically merges into the multiple-demand cognitive system.
Jefferson Ortega; Chelsea Reichert Plaska; Bernard A. Gomes; Timothy M. Ellmore
Spontaneous eye blink rate during the working memory delay period predicts task accuracy Journal Article
In: Frontiers in Psychology, vol. 13, pp. 1–11, 2022.
Spontaneous eye blink rate (sEBR) has been linked to attention and memory, specifically working memory (WM). sEBR is also related to striatal dopamine (DA) activity with schizophrenia and Parkinson's disease showing increases and decreases, respectively, in sEBR. A weakness of past studies of sEBR and WM is that correlations have been reported using blink rates taken at baseline either before or after performance of the tasks used to assess WM. The goal of the present study was to understand how fluctuations in sEBR during different phases of a visual WM task predict task accuracy. In two experiments, with recordings of sEBR collected inside and outside of a magnetic resonance imaging bore, we observed sEBR to be positively correlated with WM task accuracy during the WM delay period. We also found task-related modulation of sEBR, including higher sEBR during the delay period compared to rest, and lower sEBR during task phases (e.g., stimulus encoding) that place demands on visual attention. These results provide further evidence that sEBR could be an important predictor of WM task performance with the changes during the delay period suggesting a role in WM maintenance. The relationship of sEBR to DA activity and WM maintenance is discussed.
Soo Hyun Park; Kenji W. Koyano; Brian E. Russ; Elena N. Waidmann; David B. T. McMahon; David A. Leopold
Parallel functional subnetworks embedded in the macaque face patch system Journal Article
In: Science Advances, vol. 8, pp. 1–8, 2022.
During normal vision, our eyes provide the brain with a continuous stream of useful information about the world. How visually specialized areas of the cortex, such as face-selective patches, operate under natural modes of behavior is poorly understood. Here we report that, during the free viewing of movies, cohorts of face-selective neurons in the macaque cortex fractionate into distributed and parallel subnetworks that carry distinct information. We classified neurons into functional groups on the basis of their movie-driven coupling with functional magnetic resonance imaging time courses across the brain. Neurons from each group were distributed across multiple face patches but intermixed locally with other groups at each recording site. These findings challenge prevailing views about functional segregation in the cortex and underscore the importance of naturalistic paradigms for cognitive neuroscience.
Jordan E. Pierce; Elizabeth Clancy; Nathan M. Petro; Michael D. Dodd; Maital Neta
Task-irrelevant emotional faces impact BOLD responses more for prosaccades than antisaccades in a mixed saccade fMRI task Journal Article
In: Neuropsychologia, vol. 177, pp. 1–8, 2022.
Cognitive control allows individuals to flexibly and efficiently perform tasks by attending to relevant stimuli while inhibiting distraction from irrelevant stimuli. The antisaccade task assesses cognitive control by requiring participants to inhibit a prepotent glance towards a peripheral stimulus and generate an eye movement to the mirror image location. This task can be administered with various contextual manipulations to investigate how factors such as trial timing or emotional content interact with cognitive control. In the current study, 26 healthy adults completed a mixed antisaccade and prosaccade fMRI task that included task irrelevant emotional faces and gap/overlap timing. The results showed typical antisaccade and gap behavioral effects with greater BOLD activation in frontal and parietal brain regions for antisaccade and overlap trials. Conversely, there were no differences in behavior based on the emotion of the task irrelevant face, but trials with neutral faces had greater activation in widespread visual regions than trials with angry faces, particularly for prosaccade and overlap trials. Together, these effects suggest that a high level of cognitive control and inhibition was required throughout the task, minimizing the impact of the face presentation on saccade behavior, but leading to increased attention to the neutral faces on overlap prosaccade trials when both the task cue (look towards) and emotion stimulus (neutral, non-threatening) facilitated disinhibition of visual processing.
McKinney Pitts; Derek Evan Nee
Generalizing the control architecture of the lateral prefrontal cortex Journal Article
In: Neurobiology of Learning and Memory, vol. 195, pp. 1–14, 2022.
Cognitive control guides non-habitual, goal directed behaviors allowing us to flexibly adapt to ongoing demands. Previous work has suggested that multiple cognitive control processes exist that can be classed according to their action on present-oriented/external information versus future-oriented/internal information. These processes can be mapped onto the lateral prefrontal cortex (LPFC) such that increasingly rostral areas are involved in increasingly future-oriented/internal control processes. Whether and how such processes are organized to support goal-directed behavior remains unclear. On the one hand, the LPFC may flexibly adapt based upon demands. On the other hand, there may be a consistent control architecture such as a control hierarchy that generalizes across demands. Previous work using fMRI in humans during a comprehensive control task that engaged several control processes at once found that an area in mid-LPFC consistently exerted widespread influence throughout the LPFC. These data suggested that the mid-LPFC forms an apex of a putative control hierarchy. However, whether such an architecture generalizes across tasks remains to be tested. Here, we utilized a modified comprehensive control task designed to alter how control processes influence one another to test the generalizability of the LPFC control architecture. Univariate fMRI activations revealed distinct control-related activations relative to past work. Despite these changes, effective connectivity modeling revealed a directed architecture similar to previous findings with the mid-LPFC exerting the most widespread influences throughout LPFC. These results suggest that the fundamental control architecture of the LPFC is relatively fixed, and that different demands are accommodated through modulations of this fixed architecture.
Ignacio Polti; Matthias Nau; Raphael Kaplan; Virginie Wassenhove; Christian F. Doeller
Rapid encoding of task regularities in the human hippocampus guides sensorimotor timing Journal Article
In: eLife, vol. 11, pp. 1–22, 2022.
The brain encodes the statistical regularities of the environment in a task-specific yet flexible and generalizable format. Here, we seek to understand this process by bridging two parallel lines of research, one centered on sensorimotor timing, and the other on cognitive mapping in the hippocampal system. By combining functional magnetic resonance imaging (fMRI) with a fast-paced time-to-contact (TTC) estimation task, we found that the hippocampus signaled behavioral feedback received in each trial as well as performance improvements across trials along with reward-processing regions. Critically, it signaled performance improvements independent from the tested intervals, and its activity accounted for the trial-wise regression-to-the-mean biases in TTC estimation. This is in line with the idea that the hippocampus supports the rapid encoding of temporal context even on short time scales in a behavior-dependent manner. Our results emphasize the central role of the hippocampus in statistical learning and position it at the core of a brain-wide network updating sensorimotor representations in real time for flexible behavior.
R. T. Pramod; Michael A. Cohen; Joshua B. Tenenbaum; Nancy Kanwisher
Invariant representation of physical stability in the human brain Journal Article
In: eLife, vol. 11, pp. 1–19, 2022.
Successful engagement with the world requires the ability to predict what will happen next. Here, we investigate how the brain makes a fundamental prediction about the physical world: whether the situation in front of us is stable, and hence likely to stay the same, or unstable, and hence likely to change in the immediate future. Specifically, we ask if judgments of stability can be supported by the kinds of representations that have proven to be highly effective at visual object recognition in both machines and brains, or instead if the ability to determine the physical stability of natural scenes may require generative algorithms that simulate the physics of the world. To find out, we measured responses in both convolutional neural networks (CNNs) and the brain (using fMRI) to natural images of physically stable versus unstable scenarios. We find no evidence for generalizable representations of physical stability in either standard CNNs trained on visual object and scene classification (ImageNet), or in the human ventral visual pathway, which has long been implicated in the same process. However, in frontoparietal regions previously implicated in intuitive physical reasoning we find both scenario-invariant representations of physical stability, and higher univariate responses to unstable than stable scenes. These results demonstrate abstract representations of physical stability in the dorsal but not ventral pathway, consistent with the hypothesis that the computations underlying stability entail not just pattern classification but forward physical simulation.
Sophia Antonia Press; Stefanie C. Biehl; C. Carolyn Vatheuer; Gregor Domes; Jennifer Svaldi
Neural correlates of body image processing in binge eating disorder Journal Article
In: Journal of Psychopathology and Clinical Science, vol. 131, no. 4, pp. 350–364, 2022.
Although body image disturbances play a central role in the development, maintenance and relapse of binge eating disorder (BED), studies investigating the neural basis underlying body processing in BED are still missing. To address this gap, we conducted a preregistered (German Clinical Trials Register [Deutsches Register Klinischer Studien; DRKS], Registration DRKS00008107) combined functional magnetic resonance (fMRI)/eye tracking study in which 38 women with BED and 22 healthy controls weight-matched for overall equivalence processed images of their own bodies, an unfamiliar weight- matched body, and visually matched nonbody control stimuli while performing a one-back task. Women with BED responded with higher left fusiform body area (FBA) activity than controls during body image processing. Despite higher levels of self-reported body dissatisfaction, women with BED did not show overactivation in emotion-processing areas in response to their own body. The eye-track- ing results indicated that visual attention toward the presented stimuli was associated with increased ac- tivity in the extrastriate body area (EBA) and FBA across groups. Our results thus provide evidence for an aberrant neural processing of body images in BED and highlight the importance of controlling for visual attention in future studies assessing neuronal body processing.
Estelle Raffin; Adrien Witon; Roberto F. Salamanca-Giron; Krystel R. Huxlin; Friedhelm C. Hummel
Functional segregation within the dorsal frontoparietal network: A multimodal dynamic causal modeling study Journal Article
In: Cerebral Cortex, vol. 32, no. 15, pp. 3187–3205, 2022.
Discrimination and integration of motion direction requires the interplay of multiple brain areas. Theoretical accounts of perception suggest that stimulus-related (i.e., exogenous) and decision-related (i.e., endogenous) factors affect distributed neuronal processing at different levels of the visual hierarchy. To test these predictions, we measured brain activity of healthy participants during a motion discrimination task, using electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). We independently modeled the impact of exogenous factors (task demand) and endogenous factors (perceptual decision-making) on the activity of the motion discrimination network and applied Dynamic Causal Modeling (DCM) to both modalities. DCM for event-related potentials (DCM-ERP) revealed that task demand impacted the reciprocal connections between the primary visual cortex (V1) and medial temporal areas (V5). With practice, higher visual areas were increasingly involved, as revealed by DCM-fMRI. Perceptual decision-making modulated higher levels (e.g., V5-to-Frontal Eye Fields, FEF), in a manner predictive of performance. Our data suggest that lower levels of the visual network support early, feature-based selection of responses, especially when learning strategies have not been implemented. In contrast, perceptual decision-making operates at higher levels of the visual hierarchy by integrating sensory information with the internal state of the subject.
Johannes Rennig; Michael S. Beauchamp
Intelligibility of audiovisual sentences drives multivoxel response patterns in human superior temporal cortex Journal Article
In: NeuroImage, vol. 247, pp. 1–9, 2022.
Regions of the human posterior superior temporal gyrus and sulcus (pSTG/S) respond to the visual mouth movements that constitute visual speech and the auditory vocalizations that constitute auditory speech, and neural responses in pSTG/S may underlie the perceptual benefit of visual speech for the comprehension of noisy auditory speech. We examined this possibility through the lens of multivoxel pattern responses in pSTG/S. BOLD fMRI data was collected from 22 participants presented with speech consisting of English sentences presented in five different formats: visual-only; auditory with and without added auditory noise; and audiovisual with and without auditory noise. Participants reported the intelligibility of each sentence with a button press and trials were sorted post-hoc into those that were more or less intelligible. Response patterns were measured in regions of the pSTG/S identified with an independent localizer. Noisy audiovisual sentences with very similar physical properties evoked very different response patterns depending on their intelligibility. When a noisy audiovisual sentence was reported as intelligible, the pattern was nearly identical to that elicited by clear audiovisual sentences. In contrast, an unintelligible noisy audiovisual sentence evoked a pattern like that of visual-only sentences. This effect was less pronounced for noisy auditory-only sentences, which evoked similar response patterns regardless of intelligibility. The successful integration of visual and auditory speech produces a characteristic neural signature in pSTG/S, highlighting the importance of this region in generating the perceptual benefit of visual speech.
Noam Saadon-Grosman; Peter A. Angeli; Lauren M. DiNicola; Randy L. Buckner
A third somatomotor representation in the human cerebellum Journal Article
In: Journal of Neurophysiology, vol. 128, no. 5, pp. 1051–1073, 2022.
Seminal neurophysiological studies in the 1940s discovered two somatomotor maps in the cerebellum-an inverted anterior lobe map and an upright posterior lobe map. Both maps have been confirmed in the human using noninvasive neuroimaging with additional hints of a third map within and near to the cerebellar vermis. Here, we sought direct evidence for the third somatomotor map by using intensive, repeated functional MRI (fMRI) scanning of individuals performing movements across multiple body parts (tongue, hands, glutes, and feet). An initial discovery sample (n = 4, 4 sessions per individual including 576 separate blocks of body movements) yielded evidence for the two established cerebellar somatomotor maps, as well as evidence for a third discontinuous foot representation within the vermis. When the left versus right foot movements were directly contrasted, the third representation could be clearly distinguished from the second representation in multiple individuals. Functional connectivity from seed regions in the third somatomotor representation confirmed anatomically specific connectivity with the cerebral cortex, paralleling the patterns observed for the two well-established maps. All results were prospectively replicated in an independent dataset with new individuals (n = 4). These collective findings provide direct support for a third somatomotor representation in the vermis of the cerebellum that may be part of a third map. We discuss the relations of this candidate third map to the broader topography of the cerebellum as well as its implications for understanding the specific organization of the human cerebellar vermis where distinct zones appear functionally specialized for somatomotor and visual domains.
Patrick Sadil; Rosemary A. Cowell; David E. Huber
A modeling framework for determining modulation of neural-level tuning from non-invasive human fMRI data Journal Article
In: Communications Biology, vol. 5, no. 1, pp. 1–12, 2022.
Many neuroscience theories assume that tuning modulation of individual neurons underlies changes in human cognition. However, non-invasive fMRI lacks sufficient resolution to visualize this modulation. To address this limitation, we developed an analysis framework called Inferring Neural Tuning Modulation (INTM) for “peering inside” voxels. Precise specification of neural tuning from the BOLD signal is not possible. Instead, INTM compares theoretical alternatives for the form of neural tuning modulation that might underlie changes in BOLD across experimental conditions. The most likely form is identified via formal model comparison, with assumed parametric Normal tuning functions, followed by a non-parametric check of conclusions. We validated the framework by successfully identifying a well-established form of modulation: visual contrast-induced multiplicative gain for orientation tuned neurons. INTM can be applied to any experimental paradigm testing several points along a continuous feature dimension (e.g., direction of motion, isoluminant hue) across two conditions (e.g., with/without attention, before/after learning).
Arunava Samaddar; Brooke S. Jackson; Christopher J. Helms; Nicole A. Lazar; Jennifer E. McDowell; Cheolwoo Park
A group comparison in fMRI data using a semiparametric model under shape invariance Journal Article
In: Computational Statistics and Data Analysis, vol. 167, pp. 1–18, 2022.
In the analysis of functional magnetic resonance imaging (fMRI) data, a common type of analysis is to compare differences across scanning sessions. A challenge to direct comparisons of this type is the low signal-to-noise ratio in fMRI data. By using the property that brain signals from a task-related experiment may exhibit a similar pattern in regions of interest across participants, a semiparametric approach under shape invariance to quantify and test the differences in sessions and groups is developed. The common function is estimated with local polynomial regression and the shape invariance model parameters are estimated using evolutionary optimization methods. The efficacy of the semi-parametric approach is demonstrated on a study of brain activation changes across two sessions associated with practice-related cognitive control. The objective of the study is to evaluate neural circuitry supporting a cognitive control task, and associated practice-related changes via acquisition of blood oxygenation level dependent (BOLD) signal collected using fMRI. By using the proposed approach, BOLD signals in multiple regions of interest for control participants and participants with schizophrenia are compared as they perform a cognitive control task (known as the antisaccade task) at two sessions, and the effects of task practice in these groups are quantified.
Takafumi Sasaoka; Tokiko Harada; Daichi Sato; Nanae Michida; Hironobu Yonezawa; Masatoshi Takayama; Takahide Nouzawa; Shigeto Yamawaki
Neural basis for anxiety and anxiety-related physiological responses during a driving situation: An fMRI study Journal Article
In: Cerebral Cortex, vol. 3, pp. 1–19, 2022.
Although the exteroceptive and interoceptive prediction of a negative event increases a person's anxiety in daily life situations, the relationship between the brain mechanism of anxiety and the anxiety-related autonomic response has not been fully understood. In this functional magnetic resonance imaging (fMRI) study, we examined the neural basis of anxiety and anxiety-related autonomic responses in a daily driving situation. Participants viewed a driving video clip in the first-person perspective. During the video clip, participants were presented with a cue to indicate whether a subsequent crash could occur (attention condition) or not (safe condition). Enhanced activities in the anterior insula, bed nucleus of the stria terminalis, thalamus, and periaqueductal gray, and higher sympathetic nerve responses (pupil dilation and peripheral arterial stiffness) were triggered by the attention condition but not with the safe condition. Autonomic response-related functional connectivity was detected in the visual cortex, cerebellum, brainstem, and MCC/PCC with the right anterior insula and its adjacent regions as seed regions. Thus, the right anterior insula and adjacent regions, in collaboration with other regions play a role in eliciting anxiety based on the prediction of negative events, by mediating anxiety-related autonomic responses according to interoceptive information.
Rebekka Schröder; Eliana Faiola; Maria Fernanda Urquijo; Katharina Bey; Inga Meyhöfer; Maria Steffens; Anna-Maria Kasparbauer; Anne Ruef; Hanna Högenauer; René Hurlemann; Joseph Kambeitz; Alexandra Philipsen; Michael Wagner; Nikolaos Koutsouleris; Ulrich Ettinger
Neural correlates of smooth pursuit eye movements in schizotypy and recent onset psychosis: A multivariate pattern classification approach Journal Article
In: Schizophrenia Bulletin Open, vol. 3, no. 1, pp. 1–13, 2022.
Schizotypy refers to a set of personality traits that bear resemblance, at subclinical level, to psychosis. Despite evidence of similarity at multiple levels of analysis, direct comparisons of schizotypy and clinical psychotic disorders are rare. Therefore, we used functional magnetic resonance imaging (fMRI) to examine the neural correlates and task-based functional connectivity (psychophysiological interactions; PPI) of smooth pursuit eye movements (SPEM) in patients with recent onset psychosis (ROP; n = 34), participants with high levels of negative (HNS; n = 46) or positive (HPS; n = 41) schizotypal traits, and low-schizotypy control participants (LS; n = 61) using machine-learning. Despite strong previous evidence that SPEM is a highly reliable marker of psychosis, patients and controls could not be significantly distinguished based on SPEM performance or blood oxygen level dependent (BOLD) signal during SPEM. Classification was, however, significant for the right frontal eye field (FEF) seed region in the PPI analyses but not for seed regions in other key areas of the SPEM network. Applying the right FEF classifier to the schizotypal samples yielded decision scores between the LS and ROP groups, suggesting similarities and dissimilarities of the HNS and HPS samples with the LS and ROP groups. The very small difference between groups is inconsistent with previous studies that showed significant differences between patients with ROP and controls in both SPEM performance and underlying neural mechanisms with large effect sizes. As the current study had sufficient power to detect such differences, other reasons are discussed.
Rebekka Schröder; Kristof Keidel; Peter Trautner; Alexander Radbruch; Ulrich Ettinger
Neural mechanisms of background and velocity effects in smooth pursuit eye movements Journal Article
In: Human Brain Mapping, pp. 1–17, 2022.
Smooth pursuit eye movements (SPEM) are essential to guide behaviour in complex visual environments. SPEM accuracy is known to be degraded by the presence of a structured visual background and at higher target velocities. The aim of this preregistered study was to investigate the neural mechanisms of these robust behavioural effects. N = 33 participants performed a SPEM task with two background conditions (present and absent) at two target velocities (0.4 and 0.6 Hz). Eye movement and BOLD data were collected simultaneously. Both the presence of a structured background and faster target velocity decreased pursuit gain and increased catch-up saccade rate. Faster targets additionally increased position error. Higher BOLD response with background was found in extensive clusters in visual, parietal, and frontal areas (including the medial frontal eye fields; FEF) partially overlapping with the known SPEM network. Faster targets were associated with higher BOLD response in visual cortex and left lateral FEF. Task-based functional connectivity analyses (psychophysiological interactions; PPI) largely replicated previous results in the basic SPEM network but did not yield additional information regarding the neural underpinnings of the background and velocity effects. The results show that the presentation of visual background stimuli during SPEM induces activity in a widespread visuo-parieto-frontal network including areas contributing to cognitive aspects of oculomotor control such as medial FEF, whereas the response to higher target velocity involves visual and motor areas such as lateral FEF. Therefore, we were able to propose for the first time different functions of the medial and lateral FEF during SPEM.
Raphael Vallat; Başak Türker; Alain Nicolas; Perrine Ruby
High dream recall frequency is associated with increased creativity and default mode network connectivity Journal Article
In: Nature and Science of Sleep, vol. 14, pp. 265–275, 2022.
Introduction: Several results suggest that the frequency of dream recall is positively correlated with personality traits such as creativity and openness to experience. In addition, neuroimaging results have evidenced different neurophysiological profiles in high dream recallers (HR) and low dream recallers (LR) during both sleep and wakefulness, specifically within regions of the default mode network (DMN). These findings are consistent with the emerging view that dreaming and mind wandering pertain to the same family of spontaneous mental processes, subserved by the DMN. Methods: To further test this hypothesis, we measured the DMN functional connectivity during resting wakefulness, together with personality and cognitive abilities (including creativity) in 28 HR and 27 LR. Results: As expected, HR demonstrated a greater DMN connectivity than LR, higher scores of creativity, and no significant difference in memory abilities. However, there was no significant correlation between creativity scores and DMN connectivity. Discussion: These results further demonstrate that there are trait neurophysiological and psychological differences between individuals who frequently recall their dreams and those who do not. They support the forebrain and the DMN hypotheses of dreaming and leave open the possibility that increased activity in the DMN promotes creative-thinking during both wakefulness and sleep. Further work is needed to test whether activity in the DMN is causally associated with creative-thinking.
Ruud L. Brink; Keno Hagena; Niklas Wilming; Peter R. Murphy; Christian Büchel; Tobias H. Donner
Flexible sensory-motor mapping rules manifest in correlated variability of stimulus and action codes across the brain Journal Article
In: Neuron, vol. 111, pp. 1–14, 2022.
Humans and non-human primates can flexibly switch between different arbitrary mappings from sensation to action to solve a cognitive task. It has remained unknown how the brain implements such flexible sensory-motor mapping rules. Here, we uncovered a dynamic reconfiguration of task-specific correlated variability between sensory and motor brain regions. Human participants switched between two rules for reporting visual orientation judgments during fMRI recordings. Rule switches were either signaled explicitly or inferred by the participants from ambiguous cues. We used behavioral modeling to reconstruct the time course of their belief about the active rule. In both contexts, the patterns of correlations between ongoing fluctuations in stimulus- and action-selective activity across visual- and action-related brain regions tracked participants' belief about the active rule. The rule-specific correlation patterns broke down around the time of behavioral errors. We conclude that internal beliefs about task state are instantiated in brain-wide, selective patterns of correlated variability.
Sophia Nestmann; Daniel Wiesen; Hans-Otto Karnath; Johannes Rennig
Temporo-parietal brain regions are involved in higher order object perception Journal Article
In: NeuroImage, vol. 234, pp. 117982, 2021.
Lesions to posterior temporo-parietal brain regions are associated with deficits in perception of global, hierarchical shapes, but also with impairments in the processing of objects presented under demanding viewing conditions. Evidence from neuroimaging studies and lesion patterns observed in patients with simultanagnosia and agnosia for object orientation suggest similar brain regions to be involved in perception of global shapes and processing of objects in atypical (‘non-canonical') orientation. In a localizer experiment, we identified individual temporo-parietal brain areas involved in global shape perception and found significantly higher BOLD signals during the processing of non-canonical compared to canonical objects. In a multivariate approach, we demonstrated that posterior temporo-parietal brain areas show distinct voxel patterns for non-canonical and canonical objects and that voxel patterns of global shapes are more similar to those of objects in non-canonical compared to canonical viewing conditions. These results suggest that temporo-parietal brain areas are not only involved in global shape perception but might serve a more general mechanism of complex object perception. Our results challenge a strict attribution of object processing to the ventral visual stream by suggesting specific dorsal contributions in more demanding viewing conditions.
Bao N. Nguyen; Scott C. Kolbe; Ashika Verghese; Christine Nearchou; Allison M. McKendrick; Gary F. Egan; Trichur R. Vidyasagar
Visual search efficiency and functional visual cortical size in children with and without dyslexia Journal Article
In: Neuropsychologia, vol. 155, pp. 107819, 2021.
Dyslexia is characterised by poor reading ability. Its aetiology is probably multifactorial, with abnormal visual processing playing an important role. Among adults with normal reading ability, there is a larger representation of central visual field in the primary visual cortex (V1) in those with more efficient visuospatial attention. In this study, we tested the hypothesis that poor reading ability in school-aged children (17 children with dyslexia, 14 control children with normal reading ability) is associated with deficits in visuospatial attention using a visual search task. We corroborated the psychophysical findings with neuroimaging, by measuring the functional size of V1 in response to a central 12° visual stimulus. Consistent with other literature, visual search was impaired and less efficient in the dyslexic children, particularly with more distractor elements in the search array (p = 0.04). We also found atypical interhemispheric asymmetry in functional V1 size in the dyslexia group (p = 0.02). Reading impaired children showed poorer visual search efficiency (p = 0.01), needing more time per unit distractor (higher ms/item). Reading ability was also correlated with V1 size asymmetry (p = 0.03), such that poorer readers showed less left hemisphere bias relative to the right hemisphere. Our findings support the view that dyslexic children have abnormal visuospatial attention and interhemispheric V1 asymmetry, relative to chronological age-matched peers, and that these factors may contribute to inter-individual variation in reading performance in children.
Katya Olmos-Solis; Anouk Mariette Loon; Christian N. L. Olivers
Content or status: Frontal and posterior cortical representations of object category and upcoming task goals in working memory Journal Article
In: Cortex, vol. 135, pp. 61–77, 2021.
To optimize task sequences, the brain must differentiate between current and prospective goals. We previously showed that currently and prospectively relevant object representations in working memory can be dissociated within object-selective cortex. Based on other recent studies indicating that a range of brain areas may be involved in distinguishing between currently relevant and prospectively relevant information in working memory, here we conducted multivoxel pattern analyses of fMRI activity in additional posterior areas (specifically early visual cortex and the intraparietal sulcus) as well as frontal areas (specifically the frontal eye fields and lateral prefrontal cortex). We assessed whether these areas represent the memory content, the current versus prospective status of the memory, or both. On each trial, participants memorized an object drawn from three different categories. The object was the target for either a first task (currently relevant), a second task (prospectively relevant), or for neither task (irrelevant). The results revealed a division of labor across brain regions: While posterior areas preferentially coded for content (i.e., the category), frontal areas carried information about the current versus prospective relevance status of the memory, irrespective of the category. Intraparietal sulcus revealed both strong category- and status-sensitivity, consistent with its hub function of combining stimulus and priority signals. Furthermore, cross-decoding analyses revealed that while current and prospective representations were similar prior to search, they became dissimilar during search, in posterior as well as frontal areas. The findings provide further evidence for a dissociation between content and control networks in working memory.
Heath R. Pardoe; Samantha P. Martin; Yijun Zhao; Allan George; Hui Yuan; Jingjie Zhou; Wei Liu; Orrin Devinsky
Estimation of in-scanner head pose changes during structural MRI using a convolutional neural network trained on eye tracker video Journal Article
In: Magnetic Resonance Imaging, vol. 81, pp. 101–108, 2021.
Introduction: In-scanner head motion is a common cause of reduced image quality in neuroimaging, and causes systematic brain-wide changes in cortical thickness and volumetric estimates derived from structural MRI scans. There are few widely available methods for measuring head motion during structural MRI. Here, we train a deep learning predictive model to estimate changes in head pose using video obtained from an in-scanner eye tracker during an EPI-BOLD acquisition with participants undertaking deliberate in-scanner head movements. The predictive model was used to estimate head pose changes during structural MRI scans, and correlated with cortical thickness and subcortical volume estimates. Methods: 21 healthy controls (age 32 ± 13 years, 11 female) were studied. Participants carried out a series of stereotyped prompted in-scanner head motions during acquisition of an EPI-BOLD sequence with simultaneous recording of eye tracker video. Motion-affected and motion-free whole brain T1-weighted MRI were also obtained. Image coregistration was used to estimate changes in head pose over the duration of the EPI-BOLD scan, and used to train a predictive model to estimate head pose changes from the video data. Model performance was quantified by assessing the coefficient of determination (R2). We evaluated the utility of our technique by assessing the relationship between video-based head pose changes during structural MRI and (i) vertex-wise cortical thickness and (ii) subcortical volume estimates. Results: Video-based head pose estimates were significantly correlated with ground truth head pose changes estimated from EPI-BOLD imaging in a hold-out dataset. We observed a general brain-wide overall reduction in cortical thickness with increased head motion, with some isolated regions showing increased cortical thickness estimates with increased motion. Subcortical volumes were generally reduced in motion affected scans. Conclusions: We trained a predictive model to estimate changes in head pose during structural MRI scans using in-scanner eye tracker video. The method is independent of individual image acquisition parameters and does not require markers to be to be fixed to the patient, suggesting it may be well suited to clinical imaging and research environments. Head pose changes estimated using our approach can be used as covariates for morphometric image analyses to improve the neurobiological validity of structural imaging studies of brain development and disease.
Gabriel Pelletier; Nadav Aridan; Lesley K. Fellows; Tom Schonberg
A preferential role for ventromedial prefrontal cortex in assessing "the value of the whole" in multiattribute object evaluation Journal Article
In: Journal of Neuroscience, vol. 41, no. 23, pp. 5056–5068, 2021.
Everyday decision-making commonly involves assigning values to complex objects with multiple value-relevant attributes. Drawing on object recognition theories, we hypothesized two routes to multiattribute evaluation: Assessing the value of the whole object based on holistic attribute configuration or summing individual attribute values. In two samples of healthy human male and female participants undergoing eye tracking and functional magnetic resonance imaging (fMRI) while evaluating novel pseudo objects, we found evidence for both forms of evaluation. Fixations to and transitions between attributes differed systematically when the value of pseudo objects was associated with individual attributes or attribute configurations. Ventromedial prefrontal cortex (vmPFC) and perirhinal cortex were engaged when configural processing was required. These results converge with our recent findings that individuals with vmPFC lesions were impaired in decisions requiring configural evaluation but not when evaluating the sum of the parts. This suggests that multiattribute decision-making engages distinct evaluation mechanisms relying on partially dissociable neural substrates, depending on the relationship between attributes and value.
Samuel Planton; Stanislas Dehaene
Cerebral representation of sequence patterns across multiple presentation formats Journal Article
In: Cortex, vol. 145, pp. 13–36, 2021.
The ability to detect the abstract pattern underlying a temporal sequence of events is crucial to many human activities, including language and mathematics, but its cortical correlates remain poorly understood. It is also unclear whether repeated exposure to the same sequence of sensory stimuli is sufficient to induce the encoding of an abstract amodal representation of the pattern. Using functional MRI, we probed the existence of such abstract codes for sequential patterns, their localization in the human brain, and their relation to existing language and math-responsive networks. We used a passive sequence violation paradigm, in which a given sequence is repeatedly presented before rare deviant sequences are introduced. We presented two binary patterns, AABB and ABAB, in four presentation formats, either visual or auditory, and either cued by the identity of the stimuli or by their spatial location. Regardless of the presentation format, a habituation to the repeated pattern and a response to pattern violations were seen in a set of inferior frontal, intraparietal and temporal areas. Within language areas, such pattern-violation responses were only found in the inferior frontal gyrus (IFG), whereas all math-responsive regions responded to pattern changes. Most of these regions also responded whenever the modality or the cue changed, suggesting a general sensitivity to violation detection. Thus, the representation of sequence patterns appears to be distributed, yet to include a core set of abstract amodal regions, particularly the IFG.
Sonia Poltoratski; Kendrick Kay; Dawn Finzi; Kalanit Grill-Spector
Holistic face recognition is an emergent phenomenon of spatial processing in face-selective regions Journal Article
In: Nature Communications, vol. 12, pp. 4745, 2021.
Spatial processing by receptive fields is a core property of the visual system. However, it is unknown how spatial processing in high-level regions contributes to recognition behavior. As face inversion is thought to disrupt typical holistic processing of information in faces, we mapped population receptive fields (pRFs) with upright and inverted faces in the human visual system. Here we show that in face-selective regions, but not primary visual cortex, pRFs and overall visual field coverage are smaller and shifted downward in response to face inversion. From these measurements, we successfully predict the relative behavioral detriment of face inversion at different positions in the visual field. This correspondence between neural measurements and behavior demonstrates how spatial processing in face-selective regions may enable holistic perception. These results not only show that spatial processing in high-level visual regions is dynamically used towards recognition, but also suggest a powerful approach for bridging neural computations by receptive fields to behavior.
John R. Purcell; Andrew Jahn; Justin M. Fine; Joshua W. Brown
Neural correlates of visual attention during risky decision evidence integration Journal Article
In: NeuroImage, vol. 234, pp. 117979, 2021.
Value-based decision-making is presumed to involve a dynamic integration process that supports assessing the potential outcomes of different choice options. Decision frameworks assume the value of a decision rests on both the desirability and risk surrounding an outcome. Previous work has highlighted neural representations of risk in the human brain, and their relation to decision choice. Key neural regions including the insula and anterior cingulate cortex (ACC) have been implicated in encoding the effects of risk on decision outcomes, including approach and avoidance. Yet, it remains unknown whether these regions are involved in the dynamic integration processes that precede and drive choice, and their relationship with ongoing attention. Here, we used concurrent fMRI and eye-tracking to discern neural activation related to visual attention preceding choice between sure-thing (i.e. safe) and risky gamble options. We found activation in both dorsal ACC (dACC) and posterior insula (PI) scaled in opposite directions with the difference in attention to risky rewards relative to risky losses. PI activation also differentiated foveations on both risky options (rewards and losses) relative to a sure-thing option. These findings point to ACC involvement in ongoing evaluation of risky but higher value options. The role of PI in risky outcomes points to a more general evaluative role in the decision-making that compares both safe and risky outcomes, irrespective of potential for gains or losses.
Abhijit Rajan; Sreenivasan Meyyappan; Yuelu Liu; Immanuel Babu Henry Samuel; Bijurika Nandi; George R. Mangun; Mingzhou Ding
The microstructure of attentional control in the dorsal attention network Journal Article
In: Journal of Cognitive Neuroscience, vol. 33, no. 6, pp. 965–983, 2021.
The top–down control of attention involves command signals arising chiefly in the dorsal attention network (DAN) in frontal and parietal cortex and propagating to sensory cortex to enable the selective processing of incoming stimuli based on their behavioral relevance. Consistent with this view, the DAN is active during preparatory (anticipatory) attention for relevant events and objects, which, in vision, may be defined by different stimulus attributes including their spatial location, color, motion, or form. How this network is organized to support different forms of preparatory attention to different stimulus attributes remains unclear. We propose that, within the DAN, there exist functional microstructures (patterns of activity) specific for controlling attention based on the specific information to be attended. To test this, we contrasted preparatory attention to stimulus location (spatial attention) and to stimulus color (feature attention), and used multivoxel pattern analysis to characterize the corresponding patterns of activity within the DAN. We observed different multivoxel patterns of BOLD activation within the DAN for the control of spatial attention (attending left vs. right) and feature attention (attending red vs. green). These patterns of activity for spatial and feature attentional control showed limited overlap with each other within the DAN. Our findings thus support a model in which the DAN has different functional microstructures for distinctive forms of top–down control of visual attention.
Ryan V. Raut; Abraham Z. Snyder; Anish Mitra; Dov Yellin; Naotaka Fujii; Rafael Malach; Marcus E. Raichle
Global waves synchronize the brain's functional systems with fluctuating arousal Journal Article
In: Science Advances, vol. 7, no. 30, pp. eabf2709, 2021.
We propose and empirically support a parsimonious account of intrinsic, brain-wide spatiotemporal organization arising from traveling waves linked to arousal. We hypothesize that these waves are the predominant physiological process reflected in spontaneous functional magnetic resonance imaging (fMRI) signal fluctuations. The correlation structure ("functional connectivity") of these fluctuations recapitulates the large-scale functional organization of the brain. However, a unifying physiological account of this structure has so far been lacking. Here, using fMRI in humans, we show that ongoing arousal fluctuations are associated with global waves of activity that slowly propagate in parallel throughout the neocortex, thalamus, striatum, and cerebellum. We show that these waves can parsimoniously account for many features of spontaneous fMRI signal fluctuations, including topographically organized functional connectivity. Last, we demonstrate similar, cortex-wide propagation of neural activity measured with electrocorticography in macaques. These findings suggest that traveling waves spatiotemporally pattern brain-wide excitability in relation to arousal.
Mor Regev; Andrea R. Halpern; Adrian M. Owen; Aniruddh D. Patel; Robert J. Zatorre
Mapping specific mental content during musical imagery Journal Article
In: Cerebral Cortex, vol. 31, no. 8, pp. 3622–3640, 2021.
Humans can mentally represent auditory information without an external stimulus, but the specificity of these internal representations remains unclear. Here, we asked how similar the temporally unfolding neural representations of imagined music are compared to those during the original perceived experience. We also tested whether rhythmic motion can influence the neural representation of music during imagery as during perception. Participants first memorized six 1-min-long instrumental musical pieces with high accuracy. Functional MRI data were collected during: 1) silent imagery of melodies to the beat of a visual metronome; 2) same but while tapping to the beat; and 3) passive listening. During imagery, inter-subject correlation analysis showed that melody-specific temporal response patterns were reinstated in right associative auditory cortices. When tapping accompanied imagery, the melody-specific neural patterns were reinstated in more extensive temporal-lobe regions bilaterally. These results indicate that the specific contents of conscious experience are encoded similarly during imagery and perception in the dynamic activity of auditory cortices. Furthermore, rhythmic motion can enhance the reinstatement of neural patterns associated with the experience of complex sounds, in keeping with models of motor to sensory influences in auditory processing.
Sarah Schuster; Nicole Alexandra; Florian Hutzler; Fabio Richlan; Martin Kronbichler; Stefan Hawelka
Cloze enough? Hemodynamic effects of predictive processing during natural reading Journal Article
In: NeuroImage, vol. 228, pp. 117687, 2021.
Evidence accrues that readers form multiple hypotheses about upcoming words. The present study investigated the hemodynamic effects of predictive processing during natural reading by means of combining fMRI and eye movement recordings. In particular, we investigated the neural and behavioral correlates of precision-weighted prediction errors, which are thought to be indicative of subsequent belief updating. Participants silently read sentences in which we manipulated the cloze probability and the semantic congruency of the final word that served as an index for precision and prediction error respectively. With respect to the neural correlates, our findings indicate an enhanced activation within the left inferior frontal and middle temporal gyrus suggesting an effect of precision on prediction update in higher (lexico-)semantic levels. Despite being evident at the neural level, we did not observe any evidence that this mechanism resulted in disproportionate reading times on participants' eye movements. The results speak against discrete predictions, but favor the notion that multiple words are activated in parallel during reading. 1.
Alyssa H. Sinclair; Grace M. Manalili; Iva K. Brunec; R. Alison Adcock; Morgan D. Barense
Prediction errors disrupt hippocampal representations and update episodic memories Journal Article
In: Proceedings of the National Academy of Sciences, vol. 118, no. 51, pp. 1–12, 2021.
The brain supports adaptive behavior by generating predictions, learning from errors, and updating memories to incorporate new information. Prediction error, or surprise, triggers learning when reality contradicts expectations. Prior studies have shown that the hippocampus signals prediction errors, but the hypothesized link to memory updating has not been demonstrated. In a human functional MRI study, we elicited mnemonic prediction errors by interrupting familiar narrative videos immediately before the expected endings. We found that prediction errors reversed the relationship between univariate hippocampal activation and memory: greater hippocampal activation predicted memory preservation after expected endings, but memory updating after surprising endings. In contrast to previous studies, we show that univariate activation was insufficient for understanding hippocampal prediction error signals. We explain this surprising finding by tracking both the evolution of hippocampal activation patterns and the connectivity between the hippocampus and neuromodulatory regions. We found that hippocampal activation patterns stabilized as each narrative episode unfolded, suggesting sustained episodic representations. Prediction errors disrupted these sustained representations and the degree of disruption predicted memory updating. The relationship between hippocampal activation and subsequent memory depended on concurrent basal forebrain activation, supporting the idea that cholinergic modulation regulates attention and memory. We conclude that prediction errors create conditions that favor memory updating, prompting the hippocampus to abandon ongoing predictions and make memories malleable.
Nathan Tardiff; John D. Medaglia; Danielle S. Bassett; Sharon L. Thompson-Schill
The modulation of brain network integration and arousal during exploration Journal Article
In: NeuroImage, vol. 240, pp. 118369, 2021.
There is growing interest in how neuromodulators shape brain networks. Recent neuroimaging studies provide evidence that brainstem arousal systems, such as the locus coeruleus-norepinephrine system (LC-NE), influence functional connectivity and brain network topology, suggesting they have a role in flexibly reconfiguring brain networks in order to adapt behavior and cognition to environmental demands. To date, however, the relationship between brainstem arousal systems and functional connectivity has not been assessed within the context of a task with an established relationship between arousal and behavior, with most prior studies relying on incidental variations in arousal or pharmacological manipulation and static brain networks constructed over long periods of time. These factors have likely contributed to a heterogeneity of effects across studies. To address these issues, we took advantage of the association between LC-NE-linked arousal and exploration to probe the relationships between exploratory choice, arousal—as measured indirectly via pupil diameter—and brain network dynamics. Exploration in a bandit task was associated with a shift toward fewer, more weakly connected modules that were more segregated in terms of connectivity and topology but more integrated with respect to the diversity of cognitive systems represented in each module. Functional connectivity strength decreased, and changes in connectivity were correlated with changes in pupil diameter, in line with the hypothesis that brainstem arousal systems influence the dynamic reorganization of brain networks. More broadly, we argue that carefully aligning dynamic network analyses with task designs can increase the temporal resolution at which behaviorally- and cognitively-relevant modulations can be identified, and offer these results as a proof of concept of this approach.
Hamid B. Turker; Elizabeth Riley; Wen Ming Luh; Stan J. Colcombe; Khena M. Swallow
Estimates of locus coeruleus function with functional magnetic resonance imaging are influenced by localization approaches and the use of multi-echo data Journal Article
In: NeuroImage, vol. 236, pp. 118047, 2021.
The locus coeruleus (LC) plays a central role in regulating human cognition, arousal, and autonomic states. Efforts to characterize the LC's function in humans using functional magnetic resonance imaging have been hampered by its small size and location near a large source of noise, the fourth ventricle. We tested whether the ability to characterize LC function is improved by employing neuromelanin-T1 weighted images (nmT1) for LC localization and multi-echo functional magnetic resonance imaging (ME-fMRI) for estimating intrinsic functional connectivity (iFC). Analyses indicated that, relative to a probabilistic atlas, utilizing nmT1 images to individually localize the LC increases the specificity of seed time series and clusters in the iFC maps. When combined with independent components analysis (ME-ICA), ME-fMRI data provided significant improvements in the temporal signal to noise ratio and DVARS relative to denoised single echo data (1E-fMRI). The effects of acquiring nmT1 images and ME-fMRI data did not appear to only reflect increases in power: iFC maps for each approach overlapped only moderately. This is consistent with findings that ME-fMRI offers substantial advantages over 1E-fMRI acquisition and denoising. It also suggests that individually identifying LC with nmT1 scans is likely to reduce the influence of other nearby brainstem regions on estimates of LC function.
Renée M. Visser; Joe Bathelt; H. Steven Scholte; Merel Kindt
Robust BOLD responses to faces but not to conditioned threat: Challenging the amygdala's reputation in human fear and extinction learning Journal Article
In: Journal of Neuroscience, vol. 41, no. 50, pp. 10278–10292, 2021.
Most of our knowledge about human emotional memory comes from animal research. Based on this work, the amygdala is often labelled the brain's "fear center", but it is unclear to what degree neural circuitries underlying fear and extinction learning are conserved across species. Neuroimaging studies in humans yield conflicting findings, with many studies failing to show amygdala activation in response to learned threat. Such null-findings are often treated as resulting from MRI-specific problems related to measuring deep brain structures. Here we test this assumption in a mega-analysis of three studies on fear acquisition (n=98; 68 female) and extinction learning (n=79; 53 female). The conditioning procedure involved presentation of two pictures of faces and two pictures of houses: one of each pair was followed by an electric shock (CS+), the other one was never followed by a shock (CS-), and participants were instructed to learn these contingencies. Results revealed widespread responses to the CS+ compared to CS- in the fear network, including anterior insula, midcingulate cortex, thalamus and bed nucleus of the stria terminalis, but not the amygdala, which actually responded stronger to the CS-. Results were independent of spatial smoothing, and individual differences in trait anxiety and conditioned pupil responses. In contrast, robust amygdala activation distinguished faces from houses, refuting the idea that poor signal could account for the absence of effects. Moving forward, we suggest that apart from imaging larger samples at higher resolution, alternative statistical approaches may be employed to identify cross-species similarities in fear and extinction learning.
Clement Abbatecola; Peggy Gerardin; Kim Beneyton; Henry Kennedy; Kenneth Knoblauch
The role of unimodal feedback pathways in gender perception during activation of voice and face areas Journal Article
In: Frontiers in Systems Neuroscience, vol. 15, pp. 669256, 2021.
Cross-modal effects provide a model framework for investigating hierarchical inter-areal processing, particularly, under conditions where unimodal cortical areas receive contextual feedback from other modalities. Here, using complementary behavioral and brain imaging techniques, we investigated the functional networks participating in face and voice processing during gender perception, a high-level feature of voice and face perception. Within the framework of a signal detection decision model, Maximum likelihood conjoint measurement (MLCM) was used to estimate the contributions of the face and voice to gender comparisons between pairs of audio-visual stimuli in which the face and voice were independently modulated. Top–down contributions were varied by instructing participants to make judgments based on the gender of either the face, the voice or both modalities (N = 12 for each task). Estimated face and voice contributions to the judgments of the stimulus pairs were not independent; both contributed to all tasks, but their respective weights varied over a 40-fold range due to top–down influences. Models that best described the modal contributions required the inclusion of two different top–down interactions: (i) an interaction that depended on gender congruence across modalities (i.e., difference between face and voice modalities for each stimulus); (ii) an interaction that depended on the within modalities' gender magnitude. The significance of these interactions was task dependent. Specifically, gender congruence interaction was significant for the face and voice tasks while the gender magnitude interaction was significant for the face and stimulus tasks. Subsequently, we used the same stimuli and related tasks in a functional magnetic resonance imaging (fMRI) paradigm (N = 12) to explore the neural correlates of these perceptual processes, analyzed with Dynamic Causal Modeling (DCM) and Bayesian Model Selection. Results revealed changes in effective connectivity between the unimodal Fusiform Face Area (FFA) and Temporal Voice Area (TVA) in a fashion that paralleled the face and voice behavioral interactions observed in the psychophysical data. These findings explore the role in perception of multiple unimodal parallel feedback pathways.
Alia Afyouni; Franziska Geringswald; Bruno Nazarian; Marie-Hélène Grosbras
Brain activity during antisaccades to faces in adolescence Journal Article
In: Cerebral Cortex Communications, vol. 2, pp. 1–14, 2021.
Cognitive control and social perception both change during adolescence, but little is known of the interaction of these 2 processes. We aimed to characterize developmental changes in brain activity related to the influence of a social stimulus on cognitive control and more specifically on inhibitory control. Children (age 8–11
Sara Ajina; Kristin Jünemann; Arash Sahraie; Holly Bridge
Increased visual sensitivity and occipital activity in patients with hemianopia following vision rehabilitation Journal Article
In: Journal of Neuroscience, vol. 41, no. 28, pp. 5994–6005, 2021.
Hemianopia, loss of vision in half of the visual field, results from damage to the visual pathway posterior to the optic chiasm. Despite negative effects on quality of life, few rehabilitation options are currently available. Recently, several long-term training programs have been developed that show visual improvement within the blind field, although little is known of the underlying neural changes. Here, we have investigated functional and structural changes in the brain associated with visual rehabilitation. Seven human participants with occipital lobe damage enrolled in a visual training program to distinguish which of two intervals contained a drifting Gabor patch presented within the blind field. Participants performed;25 min of training each day for 3–6 months and undertook psychophysical tests and a magnetic resonance imaging scan before and after training. A control group undertook psychophysical tests before and after an equivalent period without training. Participants who were not at ceiling on baseline tests showed on average 9.6% improvement in Gabor detection, 8.3% in detection of moving dots, and 9.9% improvement in direction discrimination after training. Importantly, psychophysical improvement only correlated with improvement in Humphrey perimetry in the trained region of the visual field. Whole-brain analysis showed an increased neural response to moving stimuli in the blind visual field in motion area V5/hMT. Using a region-of-interest approach, training had a significant effect on the blood oxygenation level-dependent signal compared with baseline. Moreover, baseline V5/hMT activity was correlated to the amount of improvement in visual sensitivity using psychophysical and perimetry tests. This study, identifying a critical role for V5/hMT in boosting visual function, may allow us to determine which patients may benefit most from training and design adjunct interventions to increase training effects.
Tara L. Alvarez; Mitchell Scheiman; Cristian Morales; Suril Gohel; Ayushi Sangoi; Elio M. Santos; Chang Yaramothu; John Vito D'Antonio-Bertagnolli; Xiaobo Li; Bharat B. Biswal
Underlying neurological mechanisms associated with symptomatic convergence insufficiency Journal Article
In: Scientific Reports, vol. 11, pp. 6545, 2021.
Convergence insufficiency (CI) is the most common binocular vision problem, associated with blurred/double vision, headaches, and sore eyes that are exacerbated when doing prolonged near work, such as reading. The Convergence Insufficiency Neuro-mechanism Adult Population Study (NCT03593031) investigates the mechanistic neural differences between 50 binocularly normal controls (BNC) and 50 symptomatic CI participants by examining the fast and slow fusional disparity vergence systems. The fast fusional system is preprogrammed and is assessed with convergence peak velocity. The slow fusional system optimizes vergence effort and is assessed by measuring the phoria adaptation magnitude and rate. For the fast fusional system, significant differences are observed between the BNC and CI groups for convergence peak velocity, final position amplitude, and functional imaging activity within the secondary visual cortex, right cuneus, and oculomotor vermis. For the slow fusional system, the phoria adaptation magnitude and rate, and the medial cuneus functional activity, are significantly different between the groups. Significant correlations are observed between vergence peak velocity and right cuneus functional activity (p = 0.002) and the rate of phoria adaptation and medial cuneus functional activity (p = 0.02). These results map the brain-behavior of vergence. Future therapeutic interventions may consider implementing procedures that increase cuneus activity for this debilitating disorder.
Magdalena Boch; Sabrina Karl; Ronald Sladky; Ludwig Huber; Claus Lamm; Isabella C. Wagner
Tailored haemodynamic response function increases detection power of fMRI in awake dogs (Canis familiaris) Journal Article
In: NeuroImage, vol. 224, pp. 117414, 2021.
Functional magnetic resonance imaging (fMRI) of awake and unrestrained dogs (Canis familiaris) has been established as a novel opportunity for comparative neuroimaging, promising important insights into the evolutionary roots of human brain function and cognition. However, data processing and analysis pipelines are often derivatives of methodological standards developed for human neuroimaging, which may be problematic due to profound neurophysiological and anatomical differences between humans and dogs. Here, we explore whether dog fMRI studies would benefit from a tailored dog haemodynamic response function (HRF). In two independent experiments, dogs were presented with different visual stimuli. BOLD signal changes in the visual cortex during these experiments were used for (a) the identification and estimation of a tailored dog HRF, and (b) the independent validation of the resulting dog HRF estimate. Time course analyses revealed that the BOLD signal in the primary visual cortex peaked significantly earlier in dogs compared to humans, while being comparable in shape. Deriving a tailored dog HRF significantly improved the model fit in both experiments, compared to the canonical HRF used in human fMRI. Using the dog HRF yielded significantly increased activation during visual stimulation, extending from the occipital lobe to the caudal parietal cortex, the bilateral temporal cortex, into bilateral hippocampal and thalamic regions. In sum, our findings provide robust evidence for an earlier onset of the dog HRF in two visual stimulation paradigms, and suggest that using such an HRF will be important to increase fMRI detection power in canine neuroimaging. By providing the parameters of the tailored dog HRF and related code, we encourage and enable other researchers to validate whether our findings generalize to other sensory modalities and experimental paradigms.
Bartosz Bohaterewicz; Anna M. Sobczak; Igor Podolak; Bartosz Wójcik; Dagmara Mȩtel; Adrian A. Chrobak; Magdalena Fa̧frowicz; Marcin Siwek; Dominika Dudek; Tadeusz Marek
Machine learning-based identification of suicidal risk in patients with Schizophrenia using multi-level resting-state fMRI features Journal Article
In: Frontiers in Neuroscience, vol. 14, pp. 605697, 2021.
Background: Some studies suggest that as much as 40% of all causes of death in a group of patients with schizophrenia can be attributed to suicides and compared with the general population, patients with schizophrenia have an 8.5-fold greater suicide risk (SR). There is a vital need for accurate and reliable methods to predict the SR among patients with schizophrenia based on biological measures. However, it is unknown whether the suicidal risk in schizophrenia can be related to alterations in spontaneous brain activity, or if the resting-state functional magnetic resonance imaging (rsfMRI) measures can be used alongside machine learning (ML) algorithms in order to identify patients with SR. Methods: Fifty-nine participants including patients with schizophrenia with and without SR as well as age and gender-matched healthy underwent 13 min resting-state functional magnetic resonance imaging. Both static and dynamic indexes of the amplitude of low-frequency fluctuation (ALFF), the fractional amplitude of low-frequency fluctuations (fALFF), regional homogeneity as well as functional connectivity (FC) were calculated and used as an input for five machine learning algorithms: Gradient boosting (GB), LASSO, Logistic Regression (LR), Random Forest and Support Vector Machine. Results: All groups revealed different intra-network functional connectivity in ventral DMN and anterior SN. The best performance was reached for the LASSO applied to FC with an accuracy of 70% and AUROC of 0.76 (p < 0.05). Significant classification ability was also reached for GB and LR using fALFF and ALFF measures. Conclusion: Our findings suggest that SR in schizophrenia can be seen on the level of DMN and SN functional connectivity alterations. ML algorithms were able to significantly differentiate SR patients. Our results could be useful in developing neuromarkers of SR in schizophrenia based on non-invasive rsfMRI.
Marie Luise Brandi; Juha M. Lahnakoski; Johannes Kopf-Beck; Tobias Nolte; Tanja M. Brückl; Leonhard Schilbach
Imagery of negative interpersonal experiences influence the neural mechanisms of social interaction Journal Article
In: Neuropsychologia, vol. 160, pp. 107923, 2021.
Negative interpersonal experiences are a key contributor to psychiatric disorders. While previous research has shown that negative interpersonal experiences influence social cognition, less is known about the effects on participation in social interactions and the underlying neurobiology. To address this, we developed a new naturalistic version of a gaze-contingent paradigm using real video sequences of gaze behaviour that respond to the participants' gaze in real-time in order to create a believable and continuous interactive social situation. Additionally, participants listened to two autobiographical audio-scripts that guided them to imagine a recent stressful and a relaxing situation and performed the gaze-based social interaction task before and after the presentation of either the stressful or the relaxing audio-script. Our results demonstrate that the social interaction task robustly recruits brain areas with known involvement in social cognition, namely the medial prefrontal cortex, bilateral temporoparietal junction, superior temporal sulcus as well as the precuneus. Imagery of negative interpersonal experiences compared to relaxing imagery led to a prolonged change in affective state and to increased brain responses during the subsequent social interaction paradigm in the temporoparietal junction, medial prefrontal cortex, anterior cingulate cortex, precuneus and inferior frontal gyrus. Taken together this study presents a new naturalistic social interaction paradigm suitable to study the neural mechanisms of social interaction and the results demonstrate that the imagery of negative interpersonal experiences affects social interaction on neural levels.
Rotem Broday-Dvir; Rafael Malach
Resting-state fluctuations underlie free and creative verbal behaviors in the human brain Journal Article
In: Cerebral Cortex, vol. 31, no. 1, pp. 213–232, 2021.
Resting-state fluctuations are ubiquitous and widely studied phenomena of the human brain, yet we are largely in the dark regarding their function in human cognition. Here we examined the hypothesis that resting-state fluctuations underlie the generation of free and creative human behaviors. In our experiment, participants were asked to perform three voluntary verbal tasks: a verbal fluency task, a verbal creativity task, and a divergent thinking task, during functional magnetic resonance imaging scanning. Blood oxygenation level dependent (BOLD)-activity during these tasks was contrasted with a control- deterministic verbal task, in which the behavior was fully determined by external stimuli. Our results reveal that all voluntary verbal-generation responses displayed a gradual anticipatory buildup that preceded the deterministic control-related responses. Critically, the time-frequency dynamics of these anticipatory buildups were significantly correlated with resting-state fluctuations' dynamics. These correlations were not a general BOLD-related or verbal-response related result, as they were not found during the externally determined verbal control condition. Furthermore, they were located in brain regions known to be involved in language production, specifically the left inferior frontal gyrus. These results suggest a common function of resting-state fluctuations as the neural mechanism underlying the generation of free and creative behaviors in the human cortex.
Joana Carvalho; Remco J. Renken; Frans W. Cornelissen
Predictive masking of an artificial scotoma is associated with a system-wide reconfiguration of neural populations in the human visual cortex Journal Article
In: NeuroImage, vol. 245, pp. 118690, 2021.
The visual brain has the remarkable capacity to complete our percept of the world even when the information extracted from the visual scene is incomplete. This ability to predict missing information based on information from spatially adjacent regions is an intriguing attribute of healthy vision. Yet, it gains particular significance when it masks the perceptual consequences of a retinal lesion, leaving patients unaware of their partial loss of vision and ultimately delaying diagnosis and treatment. At present, our understanding of the neural basis of this masking process is limited which hinders both quantitative modeling as well as translational application. To overcome this, we asked the participants to view visual stimuli with and without superimposed artificial scotoma (AS). We used fMRI to record the associated cortical activity and applied model-based analyzes to track changes in cortical population receptive fields and connectivity in response to the introduction of the AS. We found that throughout the visual field and cortical hierarchy, pRFs shifted their preferred position towards the AS border. Moreover, extrastriate areas biased their sampling of V1 towards sections outside the AS projection zone, thereby effectively masking the AS with signals from spared portions of the visual field. We speculate that the signals that drive these system-wide population modifications originate in extrastriate visual areas and, through feedback, also reconfigure the neural populations in the earlier visual areas.
Simon Majed Ceh; Sonja Annerer-Walcher; Karl Koschutnig; Christof Körner; Andreas Fink; Mathias Benedek
Neurophysiological indicators of internal attention: An fMRI–eye-tracking coregistration study Journal Article
In: Cortex, vol. 143, pp. 29–46, 2021.
Many goal-directed, as well as spontaneous everyday activities (e.g., planning, mind-wandering), rely on an internal focus of attention. This fMRI–eye-tracking coregistration study investigated brain mechanisms and eye behavior related to internally versus externally directed cognition. Building on an established paradigm, we manipulated internal attention demands within tasks utilizing conditional stimulus masking. Internally directed cognition involved bilateral activation of the lingual gyrus and inferior parietal lobe areas as well as wide-spread deactivation of visual networks. Moreover, internally directed cognition was related to greater pupil diameter, pupil diameter variance, blink duration, fixation disparity variance, and smaller amounts of microsaccades. FMRI–eye-tracking covariation analyses further revealed that larger pupil diameter was related to increased activation of basal ganglia and lingual gyrus. It can be concluded that internally and externally directed cognition are characterized by distinct neurophysiological signatures. The observed neurophysiological differences indicate that internally directed cognition is associated with reduced processing of task-irrelevant information and increased mental load. These findings shed further light on the interplay between neural and perceptual mechanisms contributing to an internal focus of attention.