Neural Evidence of Hierarchical Cognitive Control during Haptic Processing: An fMRI Study

Gurtubay-Antolin, Ane; León-Cabrera, Patricia; Rodríguez-Fornells, Antoni · 2018 · Crossref

DOI: 10.1523/eneuro.0295-18.2018

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Summary

This study investigates the neural architecture underlying haptic monitoring during object manipulation, specifically addressing how the brain compares predicted and actual sensory inputs. Dexterous manipulation requires constant adjustment of motor commands based on somatosensory feedback, a process theorized to involve hierarchical cognitive control via lower- and higher-order corollary discharge signals. However, the specific neural hierarchy supporting this monitoring remains poorly understood. The authors aimed to identify the cross-talk between lower-order sensory regions and higher-order associative areas during the detection of haptic mismatches. The researchers employed functional magnetic resonance imaging (fMRI) in 17 participants performing a haptic discrimination task. Participants were blindfolded and palpated objects while judging whether the touched shape or texture matched a previously presented auditory cue. The design included congruent trials (matching expectation) and incongruent trials (mismatching expectation) for both shape and texture. To avoid circularity, an independent localizer task was first used to identify property-selective regions of interest (ROIs) specialized for shape or texture processing. Whole-brain analyses and psychophysiological interaction (PPI) connectivity analyses were then conducted to assess activation patterns and functional coupling during incongruent versus congruent trials. Behavioral results showed high accuracy (91% overall), with no significant difference between shape and texture blocks. fMRI results indicated that the property-selective haptic ROIs identified in the localizer task did not differentiate between expected and unexpected stimuli, suggesting they are not involved in tactile monitoring. In contrast, whole-brain analysis revealed that incongruent trials activated the left supramarginal gyrus (SMG), middle temporal cortex, and medial prefrontal cortex, regardless of whether the mismatch involved shape or texture. The left primary somatosensory area (SI) responded differently to unexpected shapes versus textures, indicating specialized detection of specific haptic mismatches. Crucially, connectivity analyses demonstrated increased functional coupling between the left SMG and SI during unexpected trials. The findings provide the first evidence of a hierarchical organization in the neural substrates of haptic monitoring. The SMG acts as a higher-order hub that compares predicted and actual somatosensory input in a modality-independent manner, while SI serves as a lower-order site for detecting specialized haptic mismatches. The enhanced connectivity between these regions during incongruent trials highlights the essential cross-talk between higher-order associative areas and lower-order sensory cortices in maintaining dexterous manipulation. This study clarifies the distinct roles of these brain regions in sensorimotor prediction and error correction.

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• multisensory crossmodal