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An interconnected group of cortical regions distributed across the primate inferotemporal cortex forms a network critical for face perception. Understanding the microarchitecture of this face network can refine mechanistic accounts of how individual areas function and interact to support visual perception. To address this, we acquire a unique dataset in macaque monkeys combining fMRI to localize face patches in vivoand then ex vivohistology to resolve their histo-architecture across cortical depths in the same individuals. Our findings reveal that face patches differ based on cytochrome oxidase (CO) and, to a lesser extent, myelin staining, with the middle lateral (ML) face patch exhibiting pronounced CO staining. Histo-architectonic differences are less pronounced when using probabilistic definitions of face patches, underscoring the importance of precision mapping integrating in vivoand ex vivomeasurements in the same individuals. This study indicates that the macaque face patch network is composed of architectonically distinct components.

How does the brain encode information about the environment? Decades of research have led to the pervasive notion that the object-processing pathway in primate cortex consists of multiple areas that are each specialized to process different object categories (such as faces, bodies, hands, non-face objects and scenes). The anatomical consistency and modularity of these regions have been interpreted as evidence that these regions are innately specialized. Here, we propose that ventral-stream modules do not represent clusters of circuits that each evolved to process some specific object category particularly important for survival, but instead reflect the effects of experience on a domain-general architecture that evolved to be able to adapt, within a lifetime, to its particular environment. Furthermore, we propose that the mechanisms underlying the development of domains are both evolutionarily old and universal across cortex. Topographic maps are fundamental, governing the development of specializations across systems, providing a framework for brain organization.

Our assignment was to review the development of the face-processing network, an assignment that carries the presupposition that a face-specific developmental program exists. We hope to cast some doubt on this assumption and instead argue that the development of face processing is guided by the same ubiquitous rules that guide the development of cortex in general.

Here we report that monkeys raised without exposure to faces did not develop face domains, but did develop domains for other categories and did show normal retinotopic organization, indicating that early face deprivation leads to a highly selective cortical processing deficit. Therefore, experience must be necessary for the formation (or maintenance) of face domains. Gaze tracking revealed that control monkeys looked preferentially at faces, even at ages prior to the emergence of face domains, but face-deprived monkeys did not, indicating that face looking is not innate. A retinotopic organization is present throughout the visual system at birth, so selective early viewing behavior could bias category-specific visual responses toward particular retinotopic representations, thereby leading to domain formation in stereotyped locations in inferotemporal cortex, without requiring category-specific templates or biases. Thus, we propose that environmental importance influences viewing behavior, viewing behavior drives neuronal activity, and neuronal activity sculpts domain formation.