The topographic organization of category-selective responses in human ventral occipitotemporal cortex (VOTC) and its relationship to regions subserving language functions is remarkably uniform across individuals. This arrangement is thought to result from the clustering of neurons responding to similar inputs, constrained by intrinsic architecture and tuned by experience. We examine the malleability of this organization in individuals with unilateral resection of VOTC during childhood for the management of drug-resistant epilepsy. In cross-sectional and longitudinal functional imaging studies, we compare the topography and neural representations of 17 category-selective regions in individuals with a VOTC resection, a 'control patient' with a resection outside VOTC, and typically developing matched controls. We demonstrate both adherence to and deviation from the standard topography, particularly with respect to the hemispheric lateralization of category-selective regions, and uncover fine-grained competitive dynamics between word- and face-selectivity over time in the single, preserved VOTC. The findings elucidate the nature and extent of cortical plasticity and highlight the potential for remodeling of extrastriate architecture and function.

Emotional expressions are an evolutionarily conserved means of social communication and are essential for social interactions. It is important to understand how anxious individuals perceive their social environments, including emotional expressions, especially with the rising prevalence of anxiety during the COVID-19 pandemic. Anxiety is often associated with an attentional bias for threat-related stimuli, such as angry faces. Yet the mechanisms by which anxiety enhances or impairs two key components of spatial attention—attentional capture and attentional disengagement—to emotional expressions are still unclear. Moreover, positive valence is often ignored in studies of threat-related attention and anxiety, despite high occurrence of happy faces during everyday social interaction. Here, we investigated the relationship between anxiety, emotional valence, and spatial attention in 574 participants across two preregistered studies. We found that happy faces capture attention more quickly than angry faces during the visual search experiment and found delayed disengagement from both angry and happy faces over neutral faces during the spatial cueing experiment. We also show that anxiety has a distinct impact on both attentional capture and disengagement of emotional faces. Together our findings highlight the role of positively valenced stimuli in attracting and holding attention and suggest that anxiety is a critical factor modulating spatial attention to emotional stimuli.

In this Journal Club, Tina Liu describes a 1988 paper that revealed the capacity of the sensory cortex for functional reorganization

The nature and extent of hemispheric lateralization and its potential for reorganization continues to be debated, although there is general agreement that there is a right hemisphere (RH) advantage for face processing in human adults. Here, we examined face processing and its lateralization in individuals with a single preserved occipitotemporal cortex (OTC), either in the RH or left hemisphere (LH), following early childhood resection for the management of drug-resistant epilepsy. The matched controls and those with a lesion outside of OTC evinced the standard superiority in processing upright over inverted faces and the reverse sensitivity to a nonface category (bicycles). In contrast, the LH and the RH patient groups were significantly less accurate than the controls and showed mild orientation sensitivities at best (and not always in the predicted directions). For the two patient groups, the accuracies of face and bicycle processing did not differ from each other and were not obviously related to performance on intermediate level global form tasks with, again, poorer thresholds for both patient groups than controls and no difference between the patient groups. These findings shed light on the complexity of hemispheric lateralization and face and nonface object processing in individuals following surgical resection of OTC. Overall, this study highlights the unique dynamics and potential for plasticity in those with childhood cortical resection.

BACKGROUND:Adolescence, a developmental period characterized by significant changes in sleep, is associated with normative increases in impulsivity. While short sleep duration has been linked to elevated impulsivity, the neural mechanism underlying the relationship between short sleep duration and elevated impulsivity remains poorly understood.METHODS:We analyzed a dataset of 7,884 drug-naive 9-10 year-olds from the Adolescent Brain Cognitive Development (ABCD) study. Among them, 5,166 have two-year follow-up neuroimaging data. Linear mixed-effects models, mediation analyses, and longitudinal mediation analyses were used to investigate the relationship between parent-reported sleep duration, impulsivity, and functional and structural connectivity between the cortex and the striatum.RESULTS:We found that less sleep duration is significantly associated with higher positive and negative urgency, which are two affect-related components of impulsivity. In addition, we observed a link between short sleep duration and reduced corticostriatal connectivity. Neural pathways associated with short sleep duration-functional connectivity between the cingulo-opercular network and the left caudate, and between the cingulo-parietal network and the right pallidum-mediated the association between sleep duration and positive urgency both at baseline and two-year follow-up. Longitudinal mediation analyses further revealed that short sleep duration and elevated positive urgency exacerbated each other through these two corticostriatal connectivities.CONCLUSIONS:These findings highlight the key role of corticostriatal connectivities in the reciprocal relationship between short sleep duration and elevated impulsivity. Given the increasing prevalence of short sleep duration in adolescents, the link between sleep duration, impulsivity, and corticostriatal connectivities has important implications for timely interventions to address impulsive problems in early adolescents.

Faces are generally assumed to be processed holistically, that is, features are represented in an integrated fashion. Similarly, pictorial representations of faces (e.g., drawings) have been shown to elicit holistic processing. Some researchers, however, have contested the concept of holistic face processing, suggesting that the perception of a face is no more than the sum of individual face parts. In the present study, we ask whether faces in paintings are processed holistically and, if so, whether this holistic processing is consistent across art styles along the realism-distortion dimension. Additionally, we seek to understand whether other factors, such as interest in art and exposure to art (e.g., visiting museums), as well as general visual recognition abilities, contribute to the potential holistic processing of faces in paintings. We found holistic face processing across stimulus sets, suggesting that holistic processing of faces in art occurs regardless of the characteristics of the art style (i.e., realism/distortion).Moreover, general interest in art showed a marginally negative correlation with holistic face processing. In contrast, general visual recognition abilities correlated positively with holistic processing, suggesting that increased capacity to process purely visual information benefits perceptual integration and grouping.

Orientation selectivity is a core property of primary visual cortex (V1) in mammals, yet patients with V1 damage can relearn orientation discrimination at trained, blind-field locations. What neural machinery underlies such recovery? Here, we explore 2 possible mechanisms involving plastic changes in 1) perilesional V1, and/or 2) visual pathways that bypass V1 and transfer information directly to extrastriate cortex, which uses it to construct orientation-selective signals. We conducted two fMRI experiments at 3T and 7T, in which 4 V1-stroke patients (age: 17–63 years, 2 females, 3 right V1 strokes) viewed oriented gratings while performing a demanding task at fixation. In Expt 1, stimuli were large (10° radius), sinusoidal gratings centered on fixation, whose orientation progressed through 16 evenly-spaced angles (0-180°) over a 24s period (Freeman et al. 2011). In Expt 2, stimuli were small (2.5° radius), oriented (45° or 135°), sinusoidal gratings, presented peripherally (7.1-8.6° eccentricity), deep within the blind or intact visual hemifield. In Expt 1, we observed reliable, orientation-selective responses in ipsilesional hMT+, which is well-known to retain activity after V1 damage (Ffytche et al., 1996; Baseler et al., 1999; Morland et al., 2004; Ajina et al., 2015; Papanikolaou et al., 2019). However, because the large grating stimulated the intact field, the blind field, and the spared visual field simultaneously, we could not rule out a contribution from peri-lesional V1. In Expt 2, we also observed reliable responses in ipsilesional hMT+ for oriented stimuli entirely inside the blind field. Ongoing analyses aim to assess the strength and selectivity of these hMT+ responses, but the fact remains that they may have been elicited in the absence of orientation-selective input from V1. This would suggest a remarkable level of plasticity for this fundamental, low-level visual feature and poses questions regarding how it arises in the residual visual circuitry.

Emotionally expressive faces evoke enhanced neural responses in multiple brain regions, a phenomenon thought to depend critically on the amygdala. This emotion-related modulation is evident even in primary visual cortex (V1), providing a potential neural substrate by which emotionally salient stimuli can affect perception. How does emotional valence information, computed in the amygdala, reach V1? Here we use high-resolution functional MRI to investigate the layer profile and retinotopic distribution of neural activity specific to emotional facial expressions. Across three experiments, human participants viewed centrally presented face stimuli varying in emotional expression and performed a gender judgment task. We found that facial valence sensitivity was evident only in superficial cortical layers and was not restricted to the retinotopic location of the stimuli, consistent with diffuse feedback-like projections from the amygdala. Together, our results provide a feedback mechanism by which the amygdala directly modulates activity at the earliest stage of visual processing. .

Attention is a fundamental cognitive function that enhances the selective processing of important stimuli. Orienting of attention can be bottom-up and stimulus-driven (exogenous attention), or top-down and goal-directed (endogenous attention). It is well established that cortical areas along the visual hierarchy are differentially modulated by exogenous and endogenous attention. During exogenous attention, modulation of stimulus-evoked activity is constant along the visual hierarchy. But for endogenous attention, the enhancement of stimulus processing increases along the visual hierarchy. The source of this enhanced activity in the visual cortex remains unknown. Here we tested the hypothesis that the human frontal eye field (FEF) differentially modulates exogenous and endogenous attention. We measured cortical activity in human observers while they performed an orientation discrimination task (Dugue et al., 2020) that required either voluntary (endogenous) or involuntary (exogenous) allocation of attention prior to the onset of a target stimulus (7T BOLD fMRI, 1.8 x 1.8 x 1.8 mm). Performance accuracy was higher when the location of the target matched the cued location (valid trials), than when the cued and target locations did not match (invalid trials). While both forms of attentional orienting induced similar behavioral cue-validity effects, they evoked different BOLD fMRI responses in FEF. In the exogenous attention task, invalid cues evoked larger BOLD response than valid cues, suggesting that FEF is involved in reorienting attention from the invalidly cued location to the target location. In contrast, in the endogenous attention task, both valid and invalid trials evoked similar BOLD responses, consistent with a role for FEF in internally directing the focus of attention. Our results demonstrate that FEF exhibits distinct patterns of BOLD activity during attentional orienting and reorienting. Ongoing studies will evaluate whether attentional modulation in FEF predicts the pattern of activity observed in visual cortex during attentional reorienting.

The visual word form area (VWFA), typically located in the left ventral occipitotemporal cortex (VOTC), emerges during reading acquisition and interfaces between high-level vision and language. Small lesions in the VWFA in adults result in pure alexia, indicating that this area is necessary for word reading. Paradoxically, large cortical resections in children which include the left VOTC, undertaken for the treatment for pharmaco-resistant epilepsy, do not necessarily lead to reading impairments. To understand the neural and behavioral consequences and the ensuing plasticity of resections encompassing the left or right, anterior or posterior, VOTC, we mapped category-selective activations (face, scene, object, and word) in four right-handed pediatric patients and 26 age-matched controls, and tested their intermediate and high-level vision. We report evidence of VWFA-related plasticity in two patients (SN: M, 12y; TC: F, 13-15y) with cortical resections encompassing the left VOTC: word activations were identified in the right VWFA, right inferior frontal and superior temporal gyrus in both patients . These findings contrast with the topography of left-lateralized word-processing network in two other longitudinal patients with resections in the left anterior VOTC (OT: M, 14y-18y) or in the right posterior VOTC (UD: M, 7-10y) and age-matched controls. Parallel to their functional reorganization of the word-processing network, we uncovered atypical representational structure of the category-selective organization in patients SN and TC. Furthermore, in longitudinal comparisons, competition between face and word representations was observed in the left VOTC in patient UD and in the right VOTC in patient TC. Finally, normal intermediate and higher-order perception was evident in all four patients, attesting to functional plasticity in visual cortex. Together, these findings reveal the sufficiency and reorganization of preserved cortex for normal word processing and provide insights into dynamic functional changes in extrastriate cortical architecture.

Emotionally expressive faces evoke enhanced neural responses in multiple brain regions, a phenomenon thought to depend critically on the amygdala. This emotion-related modulation is evident even in primary visual cortex (V1), providing a potential neural substrate by which emotionally salient stimuli can affect perception. How does emotional valence information, computed in the amygdala, reach V1? Here we use high-resolution functional MRI to investigate the layer profile and retinotopic distribution of neural activity specific to emotional facial expressions. Across three experiments, human participants viewed centrally presented face stimuli varying in emotional expression and performed a gender judgment task. We found that facial valence sensitivity was evident only in superficial cortical layers and was not restricted to the retinotopic location of the stimuli, consistent with diffuse feedback-like projections from the amygdala. Together, our results provide a feedback mechanism by which the amygdala directly modulates activity at the earliest stage of visual processing.### Competing Interest StatementThe authors have declared no competing interest.

The question of whether word and face recognition rely on overlapping or dissociable neural and cognitive mechanisms received considerable attention in the literature. In the present work, we presented words (aligned or misaligned) superimposed on faces (aligned or misaligned) and tested the interference from the unattended stimulus category on holistic processing of the attended category. In Experiment 1, we found that holistic face processing is reduced when a face was overlaid with an unattended, aligned word (processed holistically). In Experiment 2, we found a similar reduction of holistic processing for words when a word was superimposed on an unattended, aligned face (processed holistically). This reciprocal interference effect indicates a trade-off in holistic processing of the two stimuli, consistent with the idea that word and face recognition may rely on non-independent, overlapping mechanisms.

Emotional expressions are an evolutionarily conserved means of social communication. It is well-established that emotional stimuli capture attention more easily than neutral stimuli, a phenomenon often referred to as “emotional attention”. However, contradictory findings of the “threat superiority effect” and the “happy face advantage” provoke questions about how emotional valence biases attentional capture. In addition, an enduring attentional bias toward threat is commonly observed in highly anxious individuals, but the exact type of anxiety—state or trait—that modulates the attentional bias for threat has not been agreed upon. To understand how the valence of emotional faces affects attentional capture and how the type of anxiety modulates emotional attention, we preregistered and conducted an online visual search experiment via Amazon’s Mechanical Turk. Participants (n=154) searched for a unique emotional face (happy or angry) among three or seven distractor faces that were closely cropped and balanced for low-level image statistics. Consistent with the “happy face advantage”, we found an attentional bias for positive over negative valence in visual search, robust at both set sizes, in accuracy, response time, and inverse efficiency score. We also found that the anxiety ratings from the State-Trait Anxiety Inventory (STAI)—both state and trait anxiety—correlated positively with search accuracy for angry targets, but negatively with search accuracy for happy targets. Given these opposing patterns of correlation, we further computed a valence index of emotional attention as a difference in search accuracy between angry and happy targets. This valence index correlated strongly with anxiety, suggesting that participants with higher anxiety showed more threat-related attentional bias and less attentional bias to stimuli with positive valence. Together, our findings reveal the role of emotional valence in attentional capture and unveil a distinct impact of anxiety on attention to positive and threatening stimuli.

Viewing faces that are perceived as emotionally expressive evokes enhanced neural responses in multiple brain regions, a phenomenon thought to depend critically on the amygdala. This emotion-related modulation is evident even in primary visual cortex (V1), providing a potential neural substrate by which emotionally salient stimuli can affect perception. How does emotional valence information, computed in the amygdala, reach V1? Here we use high-resolution functional MRI to investigate the layer profile and retinotopic distribution of neural activity specific to emotional facial expressions. Across three experiments, human participants viewed centrally presented face stimuli varying in emotional expression and performed a gender judgment task. We found that facial valence sensitivity was evident only in superficial cortical layers and was not restricted to the retinotopic location of the stimuli, consistent with diffuse feedback-like projections from the amygdala. Together, our results provide a feedback mechanism by which the amygdala directly modulates activity at the earliest stage of visual processing.

Sleep disturbance is known to be associated with various mental disorders and often precedes the onset of mental disorders in youth. Given the increasingly acknowledged bidirectional influence between sleep disturbance and mental disorders, we aim to identify a shared neural mechanism that underlies sleep disturbance and mental disorders in preadolescents. We analyzed a dataset of 9,350 9-10 year-old children, among whom 8,845 had 1-year follow-up data, from the Adolescent Brain Cognitive Development (ABCD) study. Linear mixed-effects models, mediation analysis, and longitudinal mediation analysis were used to investigate the relationship between sleep disturbance, mental disorders, and resting-state network connectivity. Out of 186 unique connectivities, the effect of total sleep disturbance (TSP, from Sleep Disturbance Scale) and mental problems (MP, from Child Behavior Checklist) converged in the default mode network (DMN) and the dorsal attention network (DAN). Within- and between-network connectivities (DMN-DAN, DMN-DMN, DAN-DAN) mediated the relationship between baseline TSD and MP at 1-year follow-up and the relationship between baseline MP and TSD at 1-year follow-up. The pathway model in which sleep disturbance and mental problems affect each other through two anticorrelated brain networks (DMN and DAN) suggests a common neural mechanism between them. Longitudinally, a less segregated DMN and DAN is associated with negative outcomes on mental well-being and sleep disturbance a year later. These findings have important implications for the design of prevention and neurofeedback intervention for mental disorders and sleep problems.

The brain is capable of integrating signals from multiple sensory modalities. Such multisensory integration can occur in areas that are commonly considered unisensory, such as planum temporale (PT) representing the auditory association cortex. However, the roles of different afferents (feedforward vs. feedback) to PT in multisensory processing are not well understood. Our study aims to understand that by examining laminar activity patterns in different topographical subfields of human PT under unimodal and multisensory stimuli. To this end, we adopted an advanced mesoscopic (sub-millimeter) fMRI methodology at 7 T by acquiring BOLD (blood-oxygen-level-dependent contrast, which has higher sensitivity) and VAPER (integrated blood volume and perfusion contrast, which has superior laminar specificity) signal concurrently, and performed all analyses in native fMRI space benefiting from an identical acquisition between functional and anatomical images. We found a division of function between visual and auditory processing in PT and distinct feedback mechanisms in different subareas. Specifically, anterior PT was activated more by auditory inputs and received feedback modulation in superficial layers. This feedback depended on task performance and likely arose from top-down influences from higher-order multimodal areas. In contrast, posterior PT was preferentially activated by visual inputs and received visual feedback in both superficial and deep layers, which is likely projected directly from the early visual cortex. Together, these findings provide novel insights into the mechanism of multisensory interaction in human PT at the mesoscopic spatial scale.

Children with unilateral resections of ventral occipito-temporal cortex (VOTC) typically do not evince visual perceptual impairments, even when relatively large swathes of VOTC are resected. In search of possible explanations for this behavioral competence, we evaluated white matter microstructure and connectivity in eight pediatric epilepsy patients following unilateral cortical resection and 15 age-matched controls. To uncover both local and broader resection-induced effects, we analyzed tractography data using two complementary approaches. First, the microstructural properties were measured in the inferior longitudinal and the inferior fronto-occipital fasciculi, the major VOTC association tracts. Group differences were only evident in the ipsilesional, and not in the contralesional, hemisphere, and single-subject analyses revealed that these differences were limited to the site of the resection. Second, graph theory was used to characterize the connectivity of the contralesional occipito-temporal regions. There were no changes to the network properties in patients with left VOTC resections nor in patients with resections outside the VOTC, but altered network efficiency was observed in two cases with right VOTC resections. These results suggest that, in many, although perhaps not all, cases of unilateral VOTC resections in childhood, the white matter profile in the preserved contralesional hemisphere along with residual neural activity might be sufficient for normal visual perception.

The consequences of cortical resection, a treatment for humans with pharmaco-resistant epilepsy, provide a unique opportunity to advance our understanding of the nature and extent of cortical (re)organization. Despite the importance of visual processing in daily life, the neural and perceptual sequellae of occipitotemporal resections remain largely unexplored. Using psychophysical and fMRI investigations, we compared the neural and visuoperceptual profiles of 10 children or adolescents following unilateral cortical resections and their age- and gender-matched controls. Dramatically, with the exception of two individuals, both of whom had relatively greater cortical alterations, all patients showed normal perceptual performance on tasks of intermediate- and high-level vision, including face and object recognition. Consistently, again with the exception of the same two individuals, both univariate and multivariate fMRI analyses revealed normal selectivity and representational structure of category-selective regions. Furthermore, the spatial organization of category-selective regions obeyed the typical medial-to-lateral topographic organization albeit unilaterally in the structurally preserved hemisphere rather than bilaterally. These findings offer novel insights into the malleability of cortex in the pediatric population and suggest that, although experience may be necessary for the emergence of neural category-selectivity, this emergence is not necessarily contingent on the integrity of particular cortical structures. SIGNIFICANCE STATEMENT One approach to reduce seizure activity in patients with pharmaco-resistant epilepsy involves the resection of the epileptogenic focus. The impact of these resections on the perceptual behaviors and organization of visual cortex remain largely unexplored. Here, we characterized the visuoperceptual and neural profiles of ventral visual cortex in a relatively large sample of post-resection pediatric patients. Two major findings emerged. First, most patients exhibited preserved visuoperceptual performance across a wide-range of visual behaviors. Second, normal topography, magnitude, and representational structure of category-selective organization were uncovered in the spared hemisphere. These comprehensive imaging and behavioral investigations uncovered novel evidence concerning the neural representations and visual functions in children who have undergone cortical resection, and have implications for cortical plasticity more generally.