Small-object manipulation is essential in numerous human activities, although its neural bases are still essentially unknown. Recent functional imaging studies have shown that precision grasping activates a large bilateral frontoparietal network, including ventral (PMv) and dorsal (PMd) premotor areas. To dissociate the role of PMv and PMd in the control of hand and finger movements, we produced, by means of transcranial magnetic stimulation (TMS), transient virtual lesions of these two areas in both hemispheres, in healthy subjects performing a grip-lift task with their right, dominant hand. We found that a virtual lesion of PMv specifically impaired the grasping component of these movements: a lesion of either the left or right PMv altered the correct positioning of fingers on the object, a prerequisite for an efficient grasping, whereas lesioning the left, contralateral PMv disturbed the sequential recruitment of intrinsic hand muscles, all other movement parameters being unaffected by PMv lesions. Conversely, we found that a virtual lesion of the left PMd impaired the proper coupling between the grasping and lifting phases, as evidenced by the TMS-induced delay in the recruitment of proximal muscles responsible for the lifting phase; lesioning the right PMd failed to affect dominant hand movements. Finally, an analysis of the time course of these effects allowed us to demonstrate the sequential involvement of PMv and PMd in movement preparation. These results provide the first compelling evidence for a neuronal dissociation between the different phases of precision grasping in human premotor cortex.
In humans, the rostral part of the ventral premotor cortex (PMv), the homologue of F5 in monkeys, is known to be critically involved in shaping the hand to grasp objects. How does information about hand posture, that is processed in PMv, give rise to appropriate motor commands for transmission to spinal circuits controlling the hand? Whereas PMv is crucial for skilled visuomotor control of the hand, PMv sends relatively few direct corticospinal projections to spinal segments innervating hand muscles and the most likely route for PMv to contribute to the control of hand shape is through cortico-cortical connections with primary motor cortex (M1). If this is the case, we predicted that PMv-M1 interactions should be modulated specifically during precision grasping in humans. To address this issue, we investigated PMv-M1 connections by means of paired-pulse transcranial magnetic stimulation (TMS) and compared whether they were differentially modulated at rest, and during precision versus power grip. To do so, TMS was applied over M1 either in isolation or after a conditioning stimulus delivered, at different delays, over the ipsilateral PMv. For the parameters of TMS tested, we found that, at rest, PMv exerted a net inhibitory influence on M1 whereas, during power grip, this inhibition disappeared and was converted into a net facilitation during precision grip. The finding that, in humans, PMv-M1 interactions are selectively modulated during specific types of grasp provides further evidence that these connections play an important role in control of the hand.
Interactions between the ventral premotor (PMv) and the primary motor cortex (M1) are crucial for transforming an object's geometrical properties, such as its size and shape, into a motor command suitable for grasp of the object. Recently, we showed that PMv interacts with M1 in a specific fashion, depending on the hand posture. However, the functional connectivity between PMv and M1 during the preparation of an actual grasp is still unknown.To address this issue, PMv–M1 interactions were tested while subjects were preparing to grasp different visible objects requiring either a precision grip or a whole hand grasp. A conditioning–test transcranial magnetic stimulation (TMS) paradigm was used: a test stimulus was applied over M1 either in isolation or after a conditioning stimulus delivered, at different delays, over the ipsilateral PMv. Motor evoked potentials (MEPs) were recorded in the first dorsal interosseus and abductor digiti minimi muscles, which show highly differentiated activity according to grasp.While subjects prepared to grasp, delivering a conditioning PMv pulse 6 or 8 msec before a test pulse over M1 strikingly facilitated MEPs in the specific muscles that were used in the upcoming grasp. This degree of facilitation correlated with the amount of muscle activity used later in the trial to grasp the objects.The present results demonstrate that, during grasp preparation, the PMv–M1 interactions are muscle-specific. PMv appears to process the object geometrical properties relevant for the upcoming grasp, and transmits this information to M1, which in turn generates a motor command appropriate for the grasp. We also reveal that the grasp-specific facilitation resulting from PMv–M1 interactions is differently related to the upcoming grasp muscle activity than is that from paired-pulse stimulation over M1, suggesting that these two TMS paradigms assess the excitability of cortico-cortical pathways devoted to the control of grasp at two different levels.
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.
Highlights► The anterior intraparietal area (AIP) is crucial for the processing of grasp-related object properties. ► AIP receives visual information about graspable objects from both the dorsal and ventral stream. ► Reciprocal interactions between the ventral premotor (PMv) and primary motor cortex (M1) allow the motor command to be grasp-specific. ► AIP plays a causal role in influencing interactions between PMv and M1.
Transcranial magnetic stimulation (TMS) can non-invasively modulate neural activity in humans. Despite three decades of research, the spatial extent of the cortical area activated by TMS is still controversial. Moreover, how TMS interacts with task-related activity during motor behavior is unknown. Here, we applied single-pulse TMS over macaque parietal cortex while recording single-unit activity at various distances from the center of stimulation during grasping. The spatial extent of TMS-induced activation is remarkably restricted, affecting the spiking activity of single neurons in an area of cortex measuring less than 2 mm in diameter. In task-related neurons, TMS evokes a transient excitation followed by reduced activity, paralleled by a significantly longer grasping time. Furthermore, TMS-induced activity and task-related activity do not summate in single neurons. These results furnish crucial experimental evidence for the neural effects of TMS at the single-cell level and uncover the neural underpinnings of behavioral effects of TMS.
SummaryThe cortical visuomotor grasping circuit, comprising the anterior intraparietal area (AIP), ventral premotor (PMv), and primary motor cortex (M1) allows transformation of an object's physical properties into a suitable motor command for grasp [1–9]. However, little is known about how AIP contributes to the processing of grasp-related information conveyed through the cortical grasping circuit. We addressed this by studying the consequences of AIP “virtual lesions” on physiological interactions between PMv and M1 at rest or during preparation to grasp objects with either a precision grip or a whole-hand grasp. We used a conditioning-test transcranial magnetic stimulation (TMS) paradigm to test how PMv-M1 interactions [10–12] were modified by disrupting AIP function with theta-burst TMS (cTBS) [13]. At rest, AIP virtual lesions did not modify PMv-M1 interactions. In contrast, the usual muscle-specific PMv-M1 interactions that appeared during grasp preparation were significantly reduced following AIP cTBS without directly modifying corticospinal excitability. Behaviorally, disruption of AIP was also associated with a relative loss of the grasp-specific pattern of digit muscle activity. These findings suggest that grasp-related and muscle-specific PMv-M1 interactions are driven by information about object properties provided by AIP.
Functional movement disorders require attention to manifest yet patients report the abnormal movement to be out of their control. In this study we explore the phenomenon of sensory attenuation, a measure of the sense of agency for movement, in this group of patients by using a force matching task. Fourteen patients and 14 healthy control subjects were presented with forces varying from 1 to 3 N on the index finger of their left hand. Participants were required to match these forces; either by pressing directly on their own finger or by operating a robot that pressed on their finger. As expected, we found that healthy control subjects consistently overestimated the force required when pressing directly on their own finger than when operating a robot. However, patients did not, indicating a significant loss of sensory attenuation in this group of patients. These data are important because they demonstrate that a fundamental component of normal voluntary movement is impaired in patients with functional movement disorders. The loss of sensory attenuation has been correlated with the loss of sense of agency, and may help to explain why patients report that they do not experience the abnormal movement as voluntary.
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