Channels for objects and environments in macaque inferotemporal cortex

Visual information processing in the primate brain is thought to occur along two major pathways, known as the ventral and dorsal pathways. The ventral ('what') pathway has been considered a system specialized for processing visual information about object structure/shape and identity. Evidence for this view comes from wide-ranging studies based on fMRI, behavioral effects of lesions and neural recording. In particular, recording studies in the macaque have revealed strong sensitivity to object shape information, ranging in complexity from 2D local contour orientation in early visual areas to 3D local surface curvature in the inferotemporal (IT) cortex, a region comprising the final stages of the ventral pathway. While object vision has been the primary focus of research in the ventral pathway, fMRI studies relating to visual representation of places or environments (e.g. landscapes and interiors) have implicated dorsal pathway areas and the parahippocampal cortex. The goal of the research presented here was to test for the first time using neural recording whether neurons in anterior IT cortex of the macaque ventral pathway are in addition to objects also sensitive to environmental shape. Neural responses were sampled using large-scale abstract visual stimuli that resembled landscapes and interiors. Specifically, visual stimuli spanned the entire scale continuum from object-scale to environment-scale stimuli and an adaptive sampling approach was used to efficiently sample the virtually infinite span of shape space. The study revealed a surprisingly strong sensitivity to environment-scale shapes in anterior IT. Additionally, there appeared to be an anatomical segregation in stimulus preference netween two IT sub-regions. Area TEd neurons were found to be predominantly selective for environment-scale stimuli whereas neurons in STSv were almost exclusively selective for object-scale stimuli. Extensive tests confirmed that neural selectivity for environment-scale stimuli is critically dependent on 3D shape. Areas TEd and STSv have been recently described as forming separate processing channels in the ventral pathway based on anatomical connectivity evidence. Our study is the first to provide a functional distinction between these channels based on object versus environment processing