No abstract

AbstractCoordinated reach-to-grasp movements are often accompanied by rapid eye movements (saccades) that displace the desired object image relative to the retina. Parietal cortex compensates for this by updating reach goals relative to current gaze direction, but its role in the integration of oculomotor and visual orientation signals for updating grasp plans is unknown. Based on a recent perceptual experiment, we hypothesized that inferior parietal cortex (specifically supramarginal gyrus; SMG) integrates saccade and visual signals to update grasp plans in more superior parietal areas. To test this hypothesis, we employed a functional magnetic resonance adaptation paradigm, where saccades sometimes interrupted grasp preparation toward a briefly presented object that later reappeared (with the same/different orientation) just before movement. Right SMG and several parietal grasp areas, namely left anterior intraparietal sulcus (aIPS) and bilateral superior parietal lobe (SPL), met our criteria for transsaccadic orientation integration: during movement preparation, they showed task-dependent saccade modulations and, during grasp execution, they were specifically sensitive to changes in object orientation that followed saccades. Finally, SMG showed enhanced functional connectivity with both prefrontal saccade areas (consistent with oculomotor input) and aIPS / SPL (consistent with sensorimotor output). These results support the general role of parietal cortex for the integration of visuospatial perturbations, and provide specific cortical modules for the integration of oculomotor and visual signals for grasp updating.Significance StatementThe cortical mechanisms that update reach goals during eye movements are well documented, but it is not known how object features are linked to oculomotor signals when updating grasp plans. Here, we employed functional magnetic resonance imaging adaptation (fMRIa) and functional connectivity analysis to identify a cluster of inferior parietal (supramarginal gyrus) and superior parietal (intraparietal and superior parietal) regions that show functional connectivity with frontal cortex saccade centers, and also show saccade-specific modulations during unexpected changes in object / grasp orientation. This provides a network - complementary to the goal updater network - that integrates visuospatial updating into grasp plans, and may help explain some of the more complex symptoms associated with parietal damage such as constructional ataxia.

Coordinated reach-to-grasp movements are often accompanied by rapid eye movements (saccades) that displace the desired object image relative to the retina. Parietal cortex compensates for this by updating reach goals relative to current gaze direction, but its role in the integration of oculomotor and visual orientation signals for updating grasp plans is unknown. Based on a recent perceptual experiment, we hypothesized that inferior parietal cortex (specifically supramarginal gyrus [SMG]) integrates saccade and visual signals to update grasp plans in additional intraparietal/superior parietal regions. To test this hypothesis in humans (7 females, 6 males), we used a functional magnetic resonance paradigm, where saccades sometimes interrupted grasp preparation toward a briefly presented object that later reappeared (with the same/different orientation) just before movement. Right SMG and several parietal grasp regions, namely, left anterior intraparietal sulcus and bilateral superior parietal lobule, met our criteria for transsaccadic orientation integration: they showed task-dependent saccade modulations and, during grasp execution, they were specifically sensitive to changes in object orientation that followed saccades. Finally, SMG showed enhanced functional connectivity with both prefrontal saccade regions (consistent with oculomotor input) and anterior intraparietal sulcus/superior parietal lobule (consistent with sensorimotor output). These results support the general role of parietal cortex for the integration of visuospatial perturbations, and provide specific cortical modules for the integration of oculomotor and visual signals for grasp updating.

Previous neuroimaging studies have shown that inferior parietal and ventral occipital cortex are involved in the transsaccadic processing of visual object orientation. Here, we investigated whether the same areas are also involved in transsaccadic processing of a different feature, namely, spatial frequency. We employed a functional magnetic resonance imaging paradigm where participants briefly viewed a grating stimulus with a specific spatial frequency that later reappeared with the same or different frequency, after a saccade or continuous fixation. First, using a whole-brain Saccade > Fixation contrast, we localized two frontal (left precentral sulcus and right medial superior frontal gyrus), four parietal (bilateral superior parietal lobule and precuneus), and four occipital (bilateral cuneus and lingual gyri) regions. Whereas the frontoparietal sites showed task specificity, the occipital sites were also modulated in a saccade control task. Only occipital cortex showed transsaccadic feature modulations, with significant repetition enhancement in right cuneus. These observations (parietal task specificity, occipital enhancement, right lateralization) are consistent with previous transsaccadic studies. However, the specific regions differed (ventrolateral for orientation, dorsomedial for spatial frequency). Overall, this study supports a general role for occipital and parietal cortex in transsaccadic vision, with a specific role for cuneus in spatial frequency processing.