Abstract

Interacting with our immediate surroundings requires constant manipulation of objects. Dexterous manipulation depends on comparison between actual and predicted sensory input, with these predictions calculated by means of lower- and higher-order corollary discharge signals. However, there is still scarce knowledge about the hierarchy in the neural architecture supporting haptic monitoring during manipulation. The present study aimed to assess this issue focusing on the cross-talk between lower-order sensory and higher-order associative regions. We used functional magnetic resonance imaging in humans during a haptic discrimination task in which participants had to judge whether a touched shape or texture corresponded to an expected stimulus whose name was previously presented. Specialized haptic regions identified with an independent localizer task did not differ between expected and unexpected conditions, suggesting their lack of involvement in tactile monitoring. When presented stimuli did not match previous expectations, the left supramarginal gyrus, middle temporal, and medial prefrontal cortices were activated regardless of the nature of the haptic mismatch (shape/texture). The left SI responded differently to unexpected shapes and textures in line with a specialized detection of haptic mismatch. Importantly, connectivity analyses revealed that the left supramarginal gyrus and SI were more functionally coupled during unexpected trials, emphasizing their interaction. The results point for the first time to a hierarchical organization in the neural substrates underlying haptic monitoring during manipulation with the supramarginal gyrus as a higher-order hub comparing actual and predicted somatosensory input, and SI as a lower-order site involved in the detection of more specialized haptic mismatch.

SIGNIFICANCE STATEMENT The findings in the present study have important implications for the understanding of the neural architecture that supports haptic monitoring during manipulation. The results point, for the first time, to a hierarchical organization in the neural substrates underlying haptic monitoring during manipulation. In this hierarchy, the supramarginal gyrus is positioned as a higher-order region comparing predicted and actual somatosensory input, and SI as a lower-order site involved in the detection of more specialized haptic mismatches. The increased functional connectivity between the supramarginal gyrus and SI during the processing of unexpected stimuli emphasizes the cross-talk between lower-order sensory and higher-order associative regions during manipulation.