Here we report that monkeys raised without exposure to faces did not develop face patches, 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 patches, 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 towards particular retinotopic representations, thereby leading to domain formation in stereotyped locations in IT, 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.

Highlights d A generative deep neural network and a genetic algorithm evolved images guided by neuronal firing d Evolved images maximized neuronal firing in alert macaque visual cortex d Evolved images activated neurons more than large numbers of natural images d Similarity to evolved images predicts response of neurons to novel images

Face recognition is highly proficient in humans and other social primates; it emerges in infancy, but the development of the neural mechanisms supporting this behaviour is largely unknown. We use blood-volume functional MRI to monitor longitudinally the responsiveness to faces, scrambled faces, and objects in macaque inferotemporal cortex (IT) from 1 month to 2 years of age. During this time selective responsiveness to monkey faces emerges. Some functional organization is present at 1 month; face-selective patches emerge over the first year of development, and are remarkably stable once they emerge. Face selectivity is refined by a decreasing responsiveness to non-face stimuli.