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AbstractHolistic 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.

Abstract
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.

According to the influential "Two Visual Pathways" hypothesis, the cortical visual system is segregated into two pathways, with the ventral, occipitotemporal pathway subserving object perception, and the dorsal, occipitoparietal pathway subserving the visuomotor control of action. However, growing evidence suggests that the dorsal pathway also plays a functional role in object perception. In the current article, we present evidence that the dorsal pathway contributes uniquely to the perception of a range of visuospatial attributes that are not redundant with representations in ventral cortex. We describe how dorsal cortex is recruited automatically during perception, even when no explicit visuomotor response is required. Importantly, we propose that dorsal cortex may selectively process visual attributes that can inform the perception of potential actions on objects and environments, and we consider plausible developmental and cognitive mechanisms that might give rise to these representations. As such, we consider whether naturalistic stimuli, such as real-world solid objects, might engage dorsal cortex more so than simplified or artificial stimuli such as images that do not afford action, and how the use of suboptimal stimuli might limit our understanding of the functional contribution of dorsal cortex to visual perception.

Abstract The organization of category‐selective regions in ventral visual cortex is well characterized in human adults. We investigated a crucial, previously unaddressed, question about how this organization emerges developmentally. We contrasted the developmental trajectories for face‐, object‐, and place‐selective activation in the ventral visual cortex in children, adolescents, and adults. Although children demonstrated adult‐like organization in object‐ and place‐related cortex, as a group they failed to show consistent face‐selective activation in classical face regions. The lack of a consistent neural signature for faces was attributable to (1) reduced face‐selectivity and extent of activation within the regions that will become the FFA, OFA, and STS in adults, and (2) smaller volumes and considerable variability in the locus of face‐selective activation in individual children. In contrast, adolescents showed an adult‐like pattern of face‐selective activation, although it was more right‐lateralized. These findings reveal critical age‐related differences in the emergence of category‐specific functional organization in the visual cortex and support a model of brain development in which specialization emerges from interactions between experience‐dependent learning and the maturing brain.

AbstractMultiple hypotheses have been offered to explain the impaired face‐processing behavior and the accompanying underlying disruptions in neural circuitry among individuals with autism. We explored the specificity of atypical face‐processing activation and potential alterations to fusiform gyrus (FG) morphology as potential underlying mechanisms. Adolescents with high functioning autism (HFA) and age‐matched typically developing (TD) adolescents were scanned with sMRI and fMRI as they observed human and animal faces. In spite of exhibiting comparable face recognition behavior, the HFA adolescents evinced hypo‐activation throughout the face‐processing system in response to unfamiliar human, but not animal, faces. They also exhibited greater activation in affective regions of the face‐processing network in response to animal, but not human, faces. Importantly, this atypical pattern of activation in response to human faces was not related to atypical structural properties of the FG. This atypical neural response to human faces in autism may stem from abnormalities in the ability to represent the reward value of social (i.e. conspecific) stimuli.

The results leading to this publication have received funding from the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394 for the project AIMS-2-TRIALS. This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results. Any views expressed are those of the author(s) and not necessarily those of the funders.

The results leading to this publication have received funding from the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394 for the project AIMS-2-TRIALS. This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results. Any views expressed are those of the author(s) and not necessarily those of the funders.

The results leading to this publication have received funding from the Innovative Medicines Initiative 2 Joint Undertaking under grant agreement No 777394 for the project AIMS-2-TRIALS. This Joint Undertaking receives support from the European Union's Horizon 2020 research and innovation programme and EFPIA and AUTISM SPEAKS, Autistica, SFARI. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results. Any views expressed are those of the author(s) and not necessarily those of the funders.