Effector-selective modulation of the effective connectivity within frontoparietal circuits during visuomotor tasks.

Despite extensive research, the functional architecture of the subregions of the dorsal posterior parietal cortex (PPC) involved in sensorimotor processing is far from clear. Here, we draw a thorough picture of the large-scale functional organization of the PPC to disentangle the fronto-parietal networks mediating visuomotor functions. To this aim, we reanalyzed available human functional magnetic resonance imaging data collected during the execution of saccades, hand, and foot pointing, and we combined individual surface-based activation, resting-state functional connectivity, and effective connectivity analyses. We described a functional distinction between a more lateral region in the posterior intraparietal sulcus (lpIPS), preferring saccades over pointing and coupled with the frontal eye fields (FEF) at rest, and a more medial portion (mpIPS) intrinsically correlated to the dorsal premotor cortex (PMd). Dynamic causal modeling revealed feedforward-feedback loops linking lpIPS with FEF during saccades and mpIPS with PMd during pointing, with substantial differences between hand and foot. Despite an intrinsic specialization of the action-specific fronto-parietal networks, our study reveals that their functioning is finely regulated according to the effector to be used, being the dynamic interactions within those networks differently modulated when carrying out a similar movement (i.e. pointing) but with distinct effectors (i.e. hand and foot).

Multisensory integration in cortical regions responding to locomotion-related visual and somatomotor signals.

During real-world locomotion, in order to be able to move along a path or avoid an obstacle, continuous changes in self-motion direction (i.e. heading) are needed. Control of heading changes during locomotion requires the integration of multiple signals (i.e., visual, somatomotor, vestibular). Recent fMRI studies have shown that both somatomotor areas (human PEc [hPEc], human PE [hPE], primary somatosensory cortex [S-I]) and egomotion visual regions (cingulate sulcus visual area [CSv], posterior cingulate area [pCi], posterior insular cortex [PIC]) respond to either leg movements and egomotion-compatible visual stimulations, suggesting a role in the analysis of both visual attributes of egomotion and somatomotor signals with the aim of guiding locomotion. However, whether these regions are able to integrate egomotion-related visual signals with somatomotor inputs coming from leg movements during heading changes remains an open question. Here we used a combined approach of individual functional localizers and task-evoked activity by fMRI. In thirty subjects we first localized three egomotion areas (CSv, pCi, PIC) and three somatomotor regions (S-I, hPE, hPEc). Then, we tested their responses in a multisensory integration experiment combining visual and somatomotor signals relevant to locomotion in congruent or incongruent trials. We used an fMR-adaptation paradigm to explore the sensitivity to the repeated presentation of these bimodal stimuli in the six regions of interest. Results revealed that hPE, S-I and CSv showed an adaptation effect regardless of congruency, while PIC, pCi and hPEc showed sensitivity to congruency. PIC exhibited a preference for congruent trials compared to incongruent trials. Areas pCi and hPEc exhibited an adaptation effect only for congruent and incongruent trials, respectively. PIC, pCi and hPEc sensitivity to the congruency relationship between visual (locomotion-compatible) cues and (leg-related) somatomotor inputs suggests that these regions are involved in multisensory integration processes, likely in order to guide/adjust leg movements during heading changes.

Egomotion-related visual areas respond to goal-directed movements.

Integration of proprioceptive signals from the various effectors with visual feedback of self-motion from the retina is necessary for whole-body movement and locomotion. Here, we tested whether the human visual motion areas involved in processing optic flow signals simulating self-motion are also activated by goal-directed movements (as saccades or pointing) performed with different effectors (eye, hand, and foot), suggesting a role in visually guiding movements through the external environment. To achieve this aim, we used a combined approach of task-evoked activity and effective connectivity (PsychoPhysiological Interaction, PPI) by fMRI. We localized a set of six egomotion-responsive visual areas through the flow field stimulus and distinguished them into visual (pIPS/V3A, V6+ , IPSmot/VIP) and visuomotor (pCi, CSv, PIC) areas according to recent literature. We tested their response to a visuomotor task implying spatially directed delayed eye, hand, and foot movements. We observed a posterior-to-anterior gradient of preference for eye-to-foot movements, with posterior (visual) regions showing a preference for saccades, and anterior (visuomotor) regions showing a preference for foot pointing. No region showed a clear preference for hand pointing. Effective connectivity analysis showed that visual areas were more connected to each other with respect to the visuomotor areas, particularly during saccades. We suggest that visual and visuomotor egomotion regions can play different roles within a network that integrates sensory-motor signals with the aim of guiding movements in the external environment.

Lower visual field preference for the visuomotor control of limb movements in the human dorsomedial parietal cortex.

Visual cues coming from the lower visual field (VF) play an important role in the visual guidance of upper and lower limb movements. A recently described region situated in the dorsomedial parietal cortex, area hPEc (Pitzalis et al. in NeuroImage 202:116092, 2019), might have a role in integrating visually derived information with somatomotor signals to guide limb interaction with the environment. In macaque, it has been demonstrated that PEc receives visual information mostly from the lower visual field but, to date, there has been no systematic investigation of VF preference in the newly defined human homologue of macaque area PEc (hPEc). Here we examined the VF preferences of hPEc while participants performed a visuomotor task implying spatially directed delayed eye-, hand- and foot-movements towards different spatial locations within the VF. By analyzing data as a function of the different target locations towards which upcoming movements were planned (and then executed), we observed the presence of asymmetry in the vertical dimension of VF in area hPEc, being this area more strongly activated by limb movements directed towards visual targets located in the lower compared to the upper VF. This result confirms the view, first advanced in macaque monkey, that PEc is involved in processing visual information to guide body interaction with the external environment, including locomotion. We also observed a contralateral dominance for the lower VF preference in the foot selective somatomotor cortex anterior to hPEc. This result might reflect the role of this cortex (which includes areas PE and S-I) in providing highly topographically organized signals, likely useful to achieve an appropriate foot posture during locomotion.

Preference for locomotion-compatible curved paths and forward direction of self-motion in somatomotor and visual areas.

During locomotion, leg movements define the direction of walking (forward or backward) and the path one is taking (straight or curved). These aspects of locomotion produce characteristic visual motion patterns during movement. Here, we tested whether cortical regions responding to either egomotion-compatible visual motion, or leg movements, or both, are sensitive to these locomotion-relevant aspects of visual motion. We compared a curved path (typically the visual feedback of a changing direction of movement in the environment) to a linear path for simulated forward and backward motion in an event-related fMRI experiment. We used an individual surface-based approach and two functional localizers to define (1) six egomotion-related areas (V6+, V3A, intraparietal motion area [IPSmot], cingulate sulcus visual area [CSv], posterior cingulate area [pCi], posterior insular cortex [PIC]) using the flow field stimulus and (2) three leg-related cortical regions (human PEc [hPEc], human PE [hPE] and primary somatosensory cortex [S-I]) using a somatomotor task. Then, we extracted the response from all these regions with respect to the main event-related fMRI experiment, consisting of passive viewing of an optic flow stimulus, simulating a forward or backward direction of self-motion in either linear or curved path. Results showed that some regions have a significant preference for the curved path motion (hPEc, hPE, S-I, IPSmot) or a preference for the forward motion (V3A), while other regions have both a significant preference for the curved path motion and for the forward compared to backward motion (V6+, CSv, pCi). We did not find any significant effects of the present stimuli in PIC. Since controlling locomotion mainly means controlling changes of walking direction in the environment during forward self-motion, such a differential functional profile among these cortical regions suggests that they play a differentiated role in the visual guidance of locomotion.