Dataset Information

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons.

ABSTRACT: Pyramidal tract neurons (PTNs) within macaque rostral ventral premotor cortex (F5) and (M1) provide direct input to spinal circuitry and are critical for skilled movement control. Contrary to initial hypotheses, they can also be active during action observation, in the absence of any movement. A population-level understanding of this phenomenon is currently lacking. We recorded from single neurons, including identified PTNs, in (M1) (n = 187), and F5 (n = 115) as two adult male macaques executed, observed, or withheld (NoGo) reach-to-grasp actions. F5 maintained a similar representation of grasping actions during both execution and observation. In contrast, although many individual M1 neurons were active during observation, M1 population activity was distinct from execution, and more closely aligned to NoGo activity, suggesting this activity contributes to withholding of self-movement. M1 and its outputs may dissociate initiation of movement from representation of grasp in order to flexibly guide behaviour.

SUBMITTER: Jerjian SJ

PROVIDER: S-EPMC7384858 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Publications

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons.

Jerjian Steven Jack SJ Sahani Maneesh M Kraskov Alexander A

eLife 20200706

Pyramidal tract neurons (PTNs) within macaque rostral ventral premotor cortex (F5) and (M1) provide direct input to spinal circuitry and are critical for skilled movement control. Contrary to initial hypotheses, they can also be active during action observation, in the absence of any movement. A population-level understanding of this phenomenon is currently lacking. We recorded from single neurons, including identified PTNs, in (M1) (n = 187), and F5 (n = 115) as two adult male macaques executed ...[more]

PMID: 32628107

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Project description: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 8msec 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.

Project description:Reaching and grasping typically are considered to be spatially separate processes that proceed concurrently in the arm and the hand, respectively. The proximal representation in the primary motor cortex (M1) controls the arm for reaching, while the distal representation controls the hand for grasping. Many studies of M1 activity therefore have focused either on reaching to various locations without grasping different objects, or else on grasping different objects all at the same location. Here, we recorded M1 neurons in the anterior bank and lip of the central sulcus as monkeys performed more naturalistic movements, reaching toward, grasping, and manipulating four different objects in up to eight different locations. We quantified the extent to which variation in firing rates depended on location, on object, and on their interaction-all as a function of time. Activity proceeded largely in two sequential phases: the first related predominantly to the location to which the upper extremity reached, and the second related to the object about to be grasped. Both phases involved activity distributed widely throughout the sampled territory, spanning both the proximal and the distal upper extremity representation in caudal M1. Our findings indicate that naturalistic reaching and grasping, rather than being spatially segregated processes that proceed concurrently, each are spatially distributed processes controlled by caudal M1 in large part sequentially. Rather than neuromuscular processes separated in space but not time, reaching and grasping are separated more in time than in space.Significance statementReaching and grasping typically are viewed as processes that proceed concurrently in the arm and hand, respectively. The arm region in the primary motor cortex (M1) is assumed to control reaching, while the hand region controls grasping. During naturalistic reach-grasp-manipulate movements, we found, however, that neuron activity proceeds largely in two sequential phases, each spanning both arm and hand representations in M1. The first phase is related predominantly to the reach location, and the second is related to the object about to be grasped. Our findings indicate that reaching and grasping are successive aspects of a single movement. Initially the arm and the hand both are projected toward the object's location, and later both are shaped to grasp and manipulate.

Dataset Information

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons.

Publications

Movement initiation and grasp representation in premotor and primary motor cortex mirror neurons.

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