Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area

Abstract

In humans, both clinical and functional imaging studies have evidenced the critical role played by the posterior parietal cortex, and particularly by the anterior intraparietal area (AIP), in skilled hand movements. However, the exact contribution of AIP to precision grasping remains debated. Here we used transcranial magnetic stimulation (TMS) to induce virtual lesions of the left and/or right AIP in subjects performing a grip-lift task with either hand. We found that, during movement preparation, a virtual lesion of AIP had distinct consequences on precision grasping of either hand depending on its time of occurrence: TMS applied 270-220 ms before the fingers contacted the manipulandum altered specifically the hand shaping, whereas lesions induced 170-120 ms before contact time only affected the grip force scaling. The lateralization of these two processes in AIP is also strikingly different: whereas a bilateral lesion of AIP was necessary to impair hand shaping, only a unilateral lesion of the left AIP altered the grip force scaling in either hand. The present study shows that, during movement preparation, AIP is responsible for processing two distinct, temporally dissociated, precision grasping parameters, regardless of the hand in use. This indicates that the contribution of AIP to hand movements is "effector-independent," a finding that may explain the invariance of grasping movements performed with either hand.

Where One Hand Meets the Other: Limb-Specific and Action-Dependent Movement Plans Decoded from Preparatory Signals in Single Human Frontoparietal Brain Areas

“…2, Table 1), allowed us to isolate brain areas involved in movement generation and then examine with MVPA the preparatory activity (plan phase) that forms between the two trial phases (note that the [execute Ͼ preview] contrast also allowed us to even localize movement-related areas containing baseline activity levels during planning and yet still examine whether predictive movement information is represented in the corresponding spatial voxel patterns). Within this network, we focused MVPA on 11 commonly described neuroanatomical ROIs in both the left and right hemispheres (22 ROIs total), each examined in our previous studies (Gallivan et al, 2011a,b) and each previously implicated in visuomotor processing in both the human and monkey: (1) superior parieto-occipital cortex (SPOC), a general region thought to be involved in reach preparation and execution Prado et al, 2005;Cavina-Pratesi et al, 2010); (2) posterior intraparietal sulcus (pIPS), a general area involved in attention and hand movement-related processes (Calton et al, 2002;Beurze et al, 2009;Chang and Snyder, 2010;Szczepanski et al, 2010); (3) middle IPS (midIPS), an area involved in limb movements Gallivan et al, 2011a,b); (4) anterior IPS (aIPS), a region involved in hand grasping Frey et al, 2005;Tunik et al, 2005;Davare et al, 2007a); (5) an area posterior to anterior IPS (post. aIPS), an area involved in object-related processing and hand preshaping (Valyear et al, 2007;Gallivan et al, 2011b); (6) motor cortex, a region predominantly involved in contralateral limb movement (Tanji et al, 1988;Kim et al, 1993;Cisek et al, 2003) and the primary source of descending projections to spinal cord (Porter and Lemon, 1993); (7) dorsal premotor cortex (PMd), a region primarily involved in reach-related processes (Caminiti et al, 1990a,b;Pesaran et al, 2006;Cavina-Pratesi et al, 2010), although also implicated in grasping (Raos et al, 2004;Cavina-Pratesi et al, 2010); (8) ventral premotor (PMv) cortex, an ROI most often implicated in hand-related actions Graziano et al, 1994;Cavina-Pratesi et al, 2010;Davare et al, 2010); (9) supplementary motor area (SMA) and (10) preSMA, two medial frontal areas involved in internally generated actions and sequencing together limb movements (Kermadi et al, 1997;…”

“…stimulation studies in monkeys (Aizawa et al, 1990;Boudrias et al, 2010) and rodents (Brus-Ramer et al, 2009), as well as TMS studies in humans (Chen et al, 1997;Stedman et al, 1998;Tinazzi and Zanette, 1998;Foltys et al, 2001;Davare et al, 2007b), all suggest a role for ipsilateral motor cortex in limb movements. However, what remains vague across many of these studies is the specific role/function of these ipsilateral representations.…”

“…If this is the case, then transcallosal coordination with ipsilateral motor cortex by the contralateral hemisphere may simply reflect automatic, naturally occurring cortical dynamics during unimanual actions, in line with observations of trial-by-trial synchronicity in contralateral and ipsilateral M1 activity . There is also evidence suggesting that ipsilateral activity may be tied to specific features of the task (e.g., movement complexity, timing of muscle recruitment; Verstynen et al, 2005;Davare et al, 2007b) or context (Diedrichsen et al, 2012). Notably, the fact that we can discriminate differences in the intention to perform ipsilateral distal finger movements (grasping vs reaching) from preparatory motor cortex signals, similar to that shown in macaque monkeys, suggests that ipsilateral motor cortex is at some level involved in movement planning.…”

“…At the anatomical level, M1 has the capacity to directly or indirectly influence ipsilateral muscle activity through uncrossed descending projections to spinal structures (Glees and Cole, 1952), contralateral descending spinal fibers that re-cross the midline to the ipsilateral side (Rosenzweig et al, 2009), or transcallosal connections to the contralateral hemisphere (Rouiller et al, 1994). Furthermore, evidence from brain-damaged patients (Hermsdörfer et al, 1999b) and stimulation studies in both monkeys (Boudrias et al, 2010) and humans (Davare et al, 2007b) all implicate ipsilateral cortex in limb movement. However, the precise localization of stimulation effects (and certainly lesion effects) is a matter of significant debate (Xu-Wilson et al, 2011), and some lines of neurophysiological evidence from the monkey Chang et al, 2008;Soteropoulos et al, 2011) argue against a direct role for the ipsilateral hemisphere in movement generation.…”

Contact forces evoked by transcranial magnetic stimulation of the motor cortex in a multi-finger grasp

“…Moreover, M1 also seems to play a crucial role in storing previously acquired information about the load since a virtual lesion of M1 induced by repeated TMS disrupted the scaling of the grip forces based on information acquired during a previous lift ( [8]; see [34]). Similarly timed TMS of other cortical areas principally disrupted the timing of the lift phase in the case of the dorsal premotor cortex or the positioning of the fingertips in the case of the ventral premotor and parietal cortex [10,11].…”