Visual processing of manipulable objects in the ventral stream is modulated by parietal action systems

Abstract Functional object use requires the integration of visuomotor representations processed in the dorsal stream with representations of the visual form, surface texture, and the material composition of objects, processed in the ventral stream. How do regions across the ventral and dorsal stream interact in support of functional object grasping and use? Here we show that the left inferior parietal lobe exerts a direct effect on neural responses in ventral occipito-temporal cortex (OTC) during visual processing of manipulable objects. We studied a series of consecutively enrolled participants in the pre-operative phase of their neurosurgical care (N = 109) with lesions distributed throughout the left hemisphere. Participants completed a category localizer functional MRI experiment in which they viewed images of manipulable objects, animals, faces, and places. Using Voxel-based Lesion-Activity Mapping (VLAM), category-preferences in neural responses in left ventral OTC were used to predict variance in voxel-wise lesion incidence throughout the brain. This approach provides direct causal evidence about which regions outside of OTC, when lesioned, cause changes in neural responses within OTC. We found that lesions to the left anterior intraparietal sulcus and left supramarginal gyrus, two inferior parietal regions known to support object-directed grasping and manipulation, respectively, are associated with reduced neural responses for manipulable objects (compared to faces, places and animals) in the left ventral OTC. Parietal lesions do not modulate neural responses during visual processing of places in the same region of left ventral OTC, even though places elicit stronger responses in the left ventral OTC than manipulable objects. To explore the structural pathways that may mediate these effects of diaschisis, we repeated the analysis using diffusion MRI-measured white matter fiber integrity as the dependent variable (instead of lesion location). That analysis identified the descending portion of the left arcuate fasciculus as the most likely pathway mediating the parietal-to-temporal lobe diaschisis identified in the VLAM analysis. These integrated VLAM and connectometry analyses demonstrate that inputs from parietal regions supporting skilled object-directed action shape neural responses in the ventral stream when viewing manipulable objects.