Functional Resilience of the Neural Visual Recognition System Post-Pediatric Occipitotemporal Resection.

In the typically developing (TD) brain, neural representations for visual stimulus categories (e.g., faces, objects, and words) emerge in bilateral occipitotemporal cortex (OTC), albeit with weighted asymmetry; in parallel, recognition behavior continues to be refined. A fundamental question is whether two hemispheres are necessary or redundant for the emergence of neural representations and recognition behavior typically distributed across both hemispheres. The rare population of patients undergoing unilateral OTC resection in childhood offers a unique opportunity to evaluate whether neural computations for visual stimulus individuation suffice for recognition with only a single developing OTC. Here, using functional magnetic resonance imaging, we mapped category selectivity (CS) and neural representations for individual stimulus exemplars using repetition suppression (RS) in the non-resected hemisphere of pediatric OTC resection patients (n = 9) and control patients with resection outside of OTC (n = 12), as well as in both hemispheres of TD controls (n = 21). There were no univariate group differences in the magnitude of CS or RS or any multivariate differences (per representational similarity analysis) in neural activation to faces, objects, or words across groups. Notwithstanding their comparable neural profiles, accuracy of OTC resection patients on face and object recognition, but not word recognition, was statistically inferior to that of controls. The comparable neural signature of the OTC resection patients' preserved hemisphere and the other two groups highlights the resilience of the system following damage to the contralateral homologue. Critically, however, a single OTC does not suffice for normal behavior, and, thereby, implicates the necessity for two hemispheres.

Visual word processing engages a hierarchical, distributed, and bilateral cortical network.

Although the Visual Word Form Area (VWFA) in left temporal cortex is considered the pre-eminent region in visual word processing, other regions are also implicated. We examined the entire text-selective circuit, using functional MRI. Ten regions of interest (ROIs) per hemisphere were defined, which, based on clustering, grouped into early vision, high-level vision, and language clusters. We analyzed the responses of the ROIs and clusters to words, inverted words, and consonant strings using univariate, multivariate, and functional connectivity measures. Bilateral modulation by stimulus condition was evident, with a stronger effect in left hemisphere regions. Last, using graph theory, we observed that the VWFA was equivalently connected with early visual and language clusters in both hemispheres, reflecting its role as a mediator in the circuit. Although the individual ROIs and clusters bilaterally were flexibly altered by the nature of the input, stability held at the level of global circuit connectivity, reflecting the complex hierarchical distributed system serving visual text perception.

Holistic processing and face expertise after pediatric resection of occipitotemporal cortex.

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.

Idiosyncratic pupil regulation in autistic children.

Recent neuroimaging and eye tracking studies have suggested that children with autism spectrum disorder (ASD) may exhibit more variable and idiosyncratic brain responses and eye movements than typically developing (TD) children. Here we extended this research for the first time to pupillometry recordings. We successfully completed pupillometry recordings with 103 children (66 with ASD), 4.5-years-old on average, who viewed three 90 second movies, twice. We extracted their pupillary time-course for each movie, capturing their stimulus evoked pupillary responses. We then computed the correlation between the time-course of each child and those of all others in their group. This yielded an average inter-subject correlation value per child, representing how similar their pupillary responses were to all others in their group. ASD participants exhibited significantly weaker inter-subject correlations than TD participants, reliably across all three movies. Differences across groups were largest in responses to a naturalistic movie containing footage of a social interaction between two TD children. This measure enabled classification of ASD and TD children with a sensitivity of 0.82 and specificity of 0.73 when trained and tested on independent datasets. Using the largest ASD pupillometry dataset to date, we demonstrate the utility of a new technique for measuring the idiosyncrasy of pupil regulation, which can be completed even by young children with co-occurring intellectual disability. These findings reveal that a considerable subgroup of ASD children have significantly more unstable, idiosyncratic pupil regulation than TD children, indicative of more variable, weakly regulated, underlying neural activity.

Morphometrics of the preserved post-surgical hemisphere in pediatric drug-resistant epilepsy.

Importance: Structural integrity of cortex following cortical resection for epilepsy management has been previously characterized, but only in adult patients. Objective: This study sought to determine whether morphometrics of the preserved hemisphere in pediatric cortical resection patients differ from non-neurological controls. Design: This was a case-control study, from 2013-2022. Setting: This was a single-site study. Participants: 32 patients with childhood epilepsy surgery and 51 age- and gender-matched controls participated. Main Measures: We quantified morphometrics of the preserved hemisphere at the level of gross anatomy (lateral ventricle size, volume of gray and white matter). Additionally, cortical thickness, volume, and surface area were measured for 34 cortical regions segmented with the Desikan-Killiany atlas, and, last, volumes of nine subcortical regions were also quantified. Results: 13 patients with left hemisphere (LH) surgery and a preserved right hemisphere (RH) (median age/median absolute deviation of age: 15.7/1.7 yr; 6 females, 7 males) and 19 patients with RH surgery and a preserved LH (15.4/3.7 yr; 11 females, 8 males) were compared to 51 controls (14.8/4.9 yr; 24 females, 27 males). Patient groups had larger ventricles and reduced total white matter volume relative to controls, and only patients with a preserved RH, but not patients with a preserved LH, had reduced total gray matter volume relative to controls. Furthermore, patients with a preserved RH had lower cortical thickness and volume and greater surface area of several cortical regions, relative to controls. Patients with a preserved LH had no differences in thickness, volume, or area, of any of the 34 cortical regions, relative to controls. Moreover, both LH and RH patients showed reduced volumes in select subcortical structures, relative to controls. Conclusions and Relevance: That left-sided, but not right-sided, resection is associated with more pronounced reduction in cortical thickness and volume and increased cortical surface area relative to typically developing, age-matched controls suggests that the preserved RH undergoes structural plasticity to an extent not observed in cases of right-sided pediatric resection. Future work probing the association of the current findings with neuropsychological outcomes will be necessary to understand the implications of these structural findings for clinical practice.

Atypical reliance on monocular visual pathway for face and word recognition in developmental dyslexia.

Studies with individuals with developmental dyslexia (DD) have documented impaired perception of words and faces, both of which are domains of visual expertise for human adults. In this study, we examined a possible mechanism that might be associated with the impaired acquisition of visual expertise for words and faces in DD, namely, the atypical engagement of the monocular visual pathway. Participants with DD and typical readers (TR) judged whether a pair of sequentially presented unfamiliar faces or nonwords were the same or different, and the pair of stimuli were displayed in an eye-specific fashion using a stereoscope. Based on evidence of greater reliance on subcortical structures early in development, we predicted differences between the groups in the engagement of lower (monocular) versus higher (binocular) regions of the visual pathways. Whereas the TR group showed a monocular advantage for both stimulus types, the DD participants evinced a monocular advantage for faces and words that was much greater than that measured in the TRs. These findings indicate that the DD individuals have enhanced subcortical engagement and that this might arise from the failure to fine-tune cortical correlates mediating the discrimination of homogeneous exemplars in domains of expertise.

Differential functional reorganization of ventral and dorsal visual pathways following childhood hemispherectomy.

Hemispherectomy is a surgical procedure in which an entire hemisphere of a patient's brain is resected or functionally disconnected to manage seizures in individuals with drug-resistant epilepsy. Despite the extensive loss of both ventral and dorsal visual pathways in one hemisphere, pediatric patients who have undergone hemispherectomy show a remarkably high degree of perceptual function across many domains. In the current study, we sought to understand the extent to which functions of the ventral and dorsal visual pathways reorganize to the contralateral hemisphere following childhood hemispherectomy. To this end, we collected fMRI data from an equal number of left and right hemispherectomy patients who completed tasks that typically elicit lateralized responses from the ventral or the dorsal pathway, namely, word (left ventral), face (right ventral), tool (left dorsal), and global form (right dorsal) perception. Overall, there was greater evidence of functional reorganization in the ventral pathway than in the dorsal pathway. Importantly, because ventral and dorsal reorganization was tested within the very same patients, these results cannot be explained by idiosyncratic factors such as disease etiology, age at the time of surgery, or age at testing. These findings suggest that because the dorsal pathway may mature earlier, it may have a shorter developmental window of plasticity than the ventral pathway and, hence, be less malleable after perturbation.

Differential functional reorganization of ventral and dorsal visual pathways following childhood hemispherectomy.

Hemispherectomy is a surgical procedure in which an entire hemisphere of a patient's brain is resected or functionally disconnected to manage seizures in individuals with drug-resistant epilepsy. Despite the extensive loss of input from both ventral and dorsal visual pathways of one hemisphere, pediatric patients who have undergone hemispherectomy show a remarkably high degree of perceptual function across many domains. In the current study, we sought to understand the extent to which functions of the ventral and dorsal visual pathways reorganize to the contralateral hemisphere following childhood hemispherectomy. To this end, we collected fMRI data from an equal number of left and right hemispherectomy patients who completed tasks that typically elicit lateralized responses from the ventral or the dorsal pathway, namely, word (left ventral), face (right ventral), tool (left dorsal), and global form (right dorsal) perception. Overall, there was greater evidence of functional reorganization in the ventral pathway than in the dorsal pathway. Importantly, because ventral and dorsal reorganization was tested in the very same patients, these results cannot be explained by idiosyncratic factors such as disease etiology, age at the time of surgery, or age at testing. These findings suggest that because the dorsal pathway may mature earlier, it may have a shorter developmental window of plasticity than the ventral pathway and, hence, be less malleable.

Temporal asymmetries and interactions between dorsal and ventral visual pathways during object recognition.

Despite their anatomical and functional distinctions, there is growing evidence that the dorsal and ventral visual pathways interact to support object recognition. However, the exact nature of these interactions remains poorly understood. Is the presence of identity-relevant object information in the dorsal pathway simply a byproduct of ventral input? Or, might the dorsal pathway be a source of input to the ventral pathway for object recognition? In the current study, we used high-density EEG-a technique with high temporal precision and spatial resolution sufficient to distinguish parietal and temporal lobes-to characterise the dynamics of dorsal and ventral pathways during object viewing. Using multivariate analyses, we found that category decoding in the dorsal pathway preceded that in the ventral pathway. Importantly, the dorsal pathway predicted the multivariate responses of the ventral pathway in a time-dependent manner, rather than the other way around. Together, these findings suggest that the dorsal pathway is a critical source of input to the ventral pathway for object recognition.

Developmental emergence of holistic processing in word recognition.

Holistic processing (HP) of faces refers to the obligatory, simultaneous processing of the parts and their relations, and it emerges over the course of development. HP is manifest in a decrement in the perception of inverted versus upright faces and a reduction in face processing ability when the relations between parts are perturbed. Here, adopting the HP framework for faces, we examined the developmental emergence of HP in another domain for which human adults have expertise, namely, visual word processing. Children, adolescents, and adults performed a lexical decision task and we used two established signatures of HP for faces: the advantage in perception of upright over inverted words and nonwords and the reduced sensitivity to increasing parts (word length). Relative to the other groups, children showed less of an advantage for upright versus inverted trials and lexical decision was more affected by increasing word length. Performance on these HP indices was strongly associated with age and with reading proficiency. Also, the emergence of HP for word perception was not simply a result of improved visual perception over the course of development as no group differences were observed on an object decision task. These results reveal the developmental emergence of HP for orthographic input, and reflect a further instance of experience-dependent tuning of visual perception. These results also add to existing findings on the commonalities of mechanisms of word and face recognition. RESEARCH HIGHLIGHTS: Children showed less of an advantage for upright versus inverted trials compared to adolescents and adults. Relative to the other groups, lexical decision in children was more affected by increasing word length. Performance on holistic processing (HP) indices was strongly associated with age and with reading proficiency. HP emergence for word perception was not due to improved visual perception over development as there were no group differences on an object decision task.

Assessing Trial-to-Trial Variability in Auditory ERPs in Autism and Schizophrenia.

Sensory abnormalities are characteristic of autism and schizophrenia. In autism, greater trial-to-trial variability (TTV) in sensory neural responses suggest that the system is more unstable. However, these findings have only been identified in the amplitude and not in the timing of neural responses, and have not been fully explored in schizophrenia. TTV in event-related potential amplitudes and inter-trial coherence (ITC) were assessed in the auditory mismatch negativity (MMN) in autism, schizophrenia, and controls. MMN was largest in autism and smallest in schizophrenia, and TTV was greater in autism and schizophrenia compared to controls. There were no differences in ITC. Greater TTV appears to be characteristic of both autism and schizophrenia, implicating several neural mechanisms that could underlie sensory instability.

Bidirectional and parallel relationships in macaque face circuit revealed by fMRI and causal pharmacological inactivation.

Although the presence of face patches in primate inferotemporal (IT) cortex is well established, the functional and causal relationships among these patches remain elusive. In two monkeys, muscimol was infused sequentially into each patch or pair of patches to assess their respective influence on the remaining IT face network and the amygdala, as determined using fMRI. The results revealed that anterior face patches required input from middle face patches for their responses to both faces and objects, while the face selectivity in middle face patches arose, in part, from top-down input from anterior face patches. Moreover, we uncovered a parallel fundal-lateral functional organization in the IT face network, supporting dual routes (dorsal-ventral) in face processing within IT cortex as well as between IT cortex and the amygdala. Our findings of the causal relationship among the face patches demonstrate that the IT face circuit is organized into multiple functional compartments.

With childhood hemispherectomy, one hemisphere can support-but is suboptimal for-word and face recognition.

The right and left cerebral hemispheres are important for face and word recognition, respectively-a specialization that emerges over human development. The question is whether this bilateral distribution is necessary or whether a single hemisphere, be it left or right, can support both face and word recognition. Here, face and word recognition accuracy in patients (median age 16.7 y) with a single hemisphere following childhood hemispherectomy was compared against matched typical controls. In experiment 1, participants viewed stimuli in central vision. Across both face and word tasks, accuracy of both left and right hemispherectomy patients, while significantly lower than controls' accuracy, averaged above 80% and did not differ from each other. To compare patients' single hemisphere more directly to one hemisphere of controls, in experiment 2, participants viewed stimuli in one visual field to constrain initial processing chiefly to a single (contralateral) hemisphere. Whereas controls had higher word accuracy when words were presented to the right than to the left visual field, there was no field/hemispheric difference for faces. In contrast, left and right hemispherectomy patients, again, showed comparable performance to one another on both face and word recognition, albeit significantly lower than controls. Altogether, the findings indicate that a single developing hemisphere, either left or right, may be sufficiently plastic for comparable representation of faces and words. However, perhaps due to increased competition or "neural crowding," constraining cortical representations to one hemisphere may collectively hamper face and word recognition, relative to that observed in typical development with two hemispheres.

Does the brain's ventral visual pathway compute object shape?

A rich behavioral literature has shown that human object recognition is supported by a representation of shape that is tolerant to variations in an object's appearance. Such 'global' shape representations are achieved by describing objects via the spatial arrangement of their local features, or structure, rather than by the appearance of the features themselves. However, accumulating evidence suggests that the ventral visual pathway - the primary substrate underlying object recognition - may not represent global shape. Instead, ventral representations may be better described as a basis set of local image features. We suggest that this evidence forces a reevaluation of the role of the ventral pathway in object perception and posits a broader network for shape perception that encompasses contributions from the dorsal pathway.

Hyper-Sensitivity to Pitch and Poorer Prosody Processing in Adults With Autism: An ERP Study.

Individuals with autism typically experience a range of symptoms, including abnormal sensory sensitivities. However, there are conflicting reports on the sensory profiles that characterize the sensory experience in autism that often depend on the type of stimulus. Here, we examine early auditory processing to simple changes in pitch and later auditory processing of more complex emotional utterances. We measured electroencephalography in 24 adults with autism and 28 controls. First, tones (1046.5Hz/C6, 1108.7Hz/C#6, or 1244.5Hz/D#6) were repeated three times or nine times before the pitch changed. Second, utterances of delight or frustration were repeated three or six times before the emotion changed. In response to the simple pitched tones, the autism group exhibited larger mismatch negativity (MMN) after nine standards compared to controls and produced greater trial-to-trial variability (TTV). In response to the prosodic utterances, the autism group showed smaller P3 responses when delight changed to frustration compared to controls. There was no significant correlation between ERPs to pitch and ERPs to prosody. Together, this suggests that early auditory processing is hyper-sensitive in autism whereas later processing of prosodic information is hypo-sensitive. The impact the different sensory profiles have on perceptual experience in autism may be key to identifying behavioral treatments to reduce symptoms.

The Dorsal Visual Pathway Represents Object-Centered Spatial Relations for Object Recognition.

Although there is mounting evidence that input from the dorsal visual pathway is crucial for object processes in the ventral pathway, the specific functional contributions of dorsal cortex to these processes remain poorly understood. Here, we hypothesized that dorsal cortex computes the spatial relations among an object's parts, a process crucial for forming global shape percepts, and transmits this information to the ventral pathway to support object categorization. Using fMRI with human participants (females and males), we discovered regions in the intraparietal sulcus (IPS) that were selectively involved in computing object-centered part relations. These regions exhibited task-dependent functional and effective connectivity with ventral cortex, and were distinct from other dorsal regions, such as those representing allocentric relations, 3D shape, and tools. In a subsequent experiment, we found that the multivariate response of posterior (p)IPS, defined on the basis of part-relations, could be used to decode object category at levels comparable to ventral object regions. Moreover, mediation and multivariate effective connectivity analyses further suggested that IPS may account for representations of part relations in the ventral pathway. Together, our results highlight specific contributions of the dorsal visual pathway to object recognition. We suggest that dorsal cortex is a crucial source of input to the ventral pathway and may support the ability to categorize objects on the basis of global shape.SIGNIFICANCE STATEMENT Humans categorize novel objects rapidly and effortlessly. Such categorization is achieved by representing an object's global shape structure, that is, the relations among object parts. Yet, despite their importance, it is unclear how part relations are represented neurally. Here, we hypothesized that object-centered part relations may be computed by the dorsal visual pathway, which is typically implicated in visuospatial processing. Using fMRI, we identified regions selective for the part relations in dorsal cortex. We found that these regions can support object categorization, and even mediate representations of part relations in the ventral pathway, the region typically thought to support object categorization. Together, these findings shed light on the broader network of brain regions that support object categorization.

Face perception: computational insights from phylogeny.

Studies of face perception in primates elucidate the psychological and neural mechanisms that support this critical and complex ability. Recent progress in characterizing face perception across species, for example in insects and reptiles, has highlighted the ubiquity over phylogeny of this key ability for social interactions and survival. Here, we review the competence in face perception across species and the types of computation that support this behavior. We conclude that the computational complexity of face perception evinced by a species is not related to phylogenetic status and is, instead, largely a product of environmental context and social and adaptive pressures. Integrating findings across evolutionary data permits the derivation of computational principles that shed further light on primate face perception.