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

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Steven Jack Jerjian ◽  
Maneesh Sahani ◽  
Alexander Kraskov

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.

2019 ◽  
Author(s):  
Jerjian S.J. ◽  
Sahani M. ◽  
Kraskov A.

AbstractPyramidal tract neurons (PTNs) within macaque rostral ventral premotor cortex (F5) and primary motor cortex (M1) provide direct input to spinal circuitry and are critical for skilled movement control, but surprisingly, can also be active during passive action observation. We recorded from single neurons, including identified PTNs in the hand and arm area of primary motor cortex (M1) (n=189), and in premotor area F5 (n=115) of two adult male macaques, while they executed, observed, or simply withheld (NoGo) reach-to-grasp and hold actions. We found that F5 maintains a more sustained, similar representation of grasping actions during both execution and observation. In contrast, although some M1 neurons mirrored during the grasp and hold, M1 population activity during observation contained signatures of a withholding state. This suggests that M1 and its output may dissociates signals required for the initiation of movement from those associated with the representation of grasp in order to flexibly guide behaviour.Significance StatementVentral premotor cortex (area F5) maintains a similar representation of grasping actions during both execution and observation. Primary motor cortex and its outputs dissociate between movement and non-movement states.


2014 ◽  
Vol 369 (1644) ◽  
pp. 20130174 ◽  
Author(s):  
A. Kraskov ◽  
R. Philipp ◽  
S. Waldert ◽  
G. Vigneswaran ◽  
M. M. Quallo ◽  
...  

Here, we report the properties of neurons with mirror-like characteristics that were identified as pyramidal tract neurons (PTNs) and recorded in the ventral premotor cortex (area F5) and primary motor cortex (M1) of three macaque monkeys. We analysed the neurons’ discharge while the monkeys performed active grasp of either food or an object, and also while they observed an experimenter carrying out a similar range of grasps. A considerable proportion of tested PTNs showed clear mirror-like properties (52% F5 and 58% M1). Some PTNs exhibited ‘classical’ mirror neuron properties, increasing activity for both execution and observation, while others decreased their discharge during observation (‘suppression mirror-neurons’). These experiments not only demonstrate the existence of PTNs as mirror neurons in M1, but also reveal some interesting differences between M1 and F5 mirror PTNs. Although observation-related changes in the discharge of PTNs must reach the spinal cord and will include some direct projections to motoneurons supplying grasping muscles, there was no EMG activity in these muscles during action observation. We suggest that the mirror neuron system is involved in the withholding of unwanted movement during action observation. Mirror neurons are differentially recruited in the behaviour that switches rapidly between making your own movements and observing those of others.


2017 ◽  
Author(s):  
Juan A. Gallego ◽  
Matthew G. Perich ◽  
Stephanie N. Naufel ◽  
Christian Ethier ◽  
Sara A. Solla ◽  
...  

AbstractHow do populations of cortical neurons have the flexibility to perform different functions? We investigated this question in primary motor cortex (M1), where populations of neurons are able to generate a rich repertoire of motor behaviors. We recorded neural activity while monkeys performed a variety of wrist and reach-to-grasp motor tasks, each requiring a different pattern of neural activity. We characterized the flexibility of M1 movement control by comparing the “neural modes” that capture covariation across neurons, believed to arise from network connectivity. We found large similarities in the structure of the neural modes across tasks, as well as striking similarities in their temporal activation dynamics. These similarities were only apparent at the population level. Moreover, a subset of these well-preserved modes captured a task-independent mapping onto muscle commands. We hypothesize that this system of flexibly combined, stable neural modes gives M1 the flexibility to generate our wide-ranging behavioral repertoire.


2017 ◽  
Author(s):  
Jonathan A Michaels ◽  
Benjamin Dann ◽  
Rijk W Intveld ◽  
Hansjörg Scherberger

AbstractOur voluntary grasping actions lie on a continuum between immediate action and waiting for the right moment, depending on the context. Therefore, studying grasping requires investigating how preparation time affects this process. Two macaque monkeys (Macaca mulatta) performed a grasping task with a short instruction followed by an immediate or delayed go cue (0-1300 ms) while we recorded in parallel from neurons in the hand area (F5) of the ventral premotor cortex and the anterior intraparietal area (AIP). Initial population dynamics followed a fixed trajectory in the neural state space unique to each grip type, reflecting unavoidable preparation, then diverged depending on the delay. Although similar types of single unit responses were present in both areas, population activity in AIP stabilized within a unique memory state while F5 activity continued to evolve, tracking subjective anticipation of the go cue. Intriguingly, activity during movement initiation clustered into two trajectory clusters, corresponding to movements that were either ‘as fast as possible’ or withheld movements, demonstrating a widespread state shift in the fronto-parietal grasping network when movements must be withheld. Our results reveal how dissociation between static and dynamic components of movement preparation as well as differentiation between cortical areas is possible through population level analysis.Significance StatementMany of our movements must occur with no warning, while others we can prepare in advance. Yet, it’s unclear how planning for movements along the spectrum between these two situations differs in the brain. Two macaque monkeys made reach to grasp movements after varying amounts of preparation time while we recorded from premotor and parietal cortex. We found that the initial response to a grasp instruction was specific to the required movement, but not the preparation time, reflecting required processing. However, when more preparation time was given, neural activity achieved unique states that likely related to withholding movements and anticipation of movement, which was more prevalent in premotor cortex, suggesting differing roles of premotor and parietal cortex in grasp planning.


2005 ◽  
Vol 19 (1) ◽  
pp. 4-13 ◽  
Author(s):  
Valerie M. Pomeroy ◽  
Christopher A. Clark ◽  
J. Simon G. Miller ◽  
Jean-Claude Baron ◽  
Hugh S. Markus ◽  
...  

Recovery of upper limb movement control after stroke might be enhanced by repetitive goal-directed functional activities. Providing such activity is challenging in the presence of severe paresis. A possible new approach is based on the discovery of mirror neurons in the monkey cortical area F5, which are active both in observing and executing a movement. Indirect evidence for a comparable human “mirror neurone system” is provided by functional imaging. The primary motor cortex, the premotor cortex, other brain areas, and muscles appropriate for the action being observed are probably activated in healthy volunteers observing another’s movement. These findings raise the hypothesis that observation of another’s movement might train the movement execution system of stroke patients who have severe paresis to bring them to the point at which they could actively participate in rehabilitation consisting of goal-directed activities. The point of providing an observation therapy would be to facilitate the voluntary production of movement; therefore, the condition of interest would be observation with intent to imitate. However, there is as yet insufficient evidence to enable the testing of this hypothesis in stroke patients. Studies in normal subjects are needed to determine which brain sites are activated in response to observation with intent to imitate. Studies in stroke subjects are needed to determine how activation is affected after damage to different brain areas. The information from such studies should aid identification of those stroke patients who might be most likely to benefit from observation to imitate and therefore guide phase I clinical studies.


2019 ◽  
Author(s):  
S.J. Jerjian ◽  
R.N. Lemon ◽  
A. Kraskov

ABSTRACTNeurons in the primate motor cortex, including identified pyramidal tract neurons projecting to the spinal cord, respond to the observation of others’ actions, yet this does not cause movement in the observer. Here, we investigated changes in spinal excitability during action observation by monitoring short latency electromyographic responses produced by single shocks delivered directly to the pyramidal tract. Responses in hand and digit muscles were recorded from two adult rhesus macaques while they performed, observed or withheld reach-to-grasp and hold actions. We found modest grasp-specific facilitation of hand muscle responses during hand shaping for grasp, which persisted when the grasp was predictable but obscured from the monkey’s vision. We also found evidence of a more general inhibition before observed movement onset, and the size of this inhibition effect was comparable to the inhibition after an explicit NoGo signal. These results confirm that the spinal circuitry controlling hand muscles is modulated during action observation, and this may be driven by internal representations of actions. The relatively modest changes in spinal excitability during observation suggest net corticospinal outflow exerts only minor, sub-threshold changes on hand motoneuron pools, thereby preventing any overflow of mirror activity into overt movement.


1998 ◽  
Vol 21 (4) ◽  
pp. 527-528 ◽  
Author(s):  
Giacomo Rizzolatti

The evolutionary continuity between the prespeech functions of premotor cortex and its new linguistic functions, the main thesis of MacNeilage's target article, is confirmed by the recent discovery of “mirror” neurons in monkeys and a corresponding action-observation/action-execution matching system in humans. Physiological data (and other considerations) appear to indicate, however, that brachiomanual gestures played a greater role in language evolution than MacNeilage would like to admit.


Author(s):  
Davide Albertini ◽  
Marco Lanzilotto ◽  
Monica Maranesi ◽  
Luca Bonini

The neural processing of others' observed actions recruits a large network of brain regions (the action observation network, AON), in which frontal motor areas are thought to play a crucial role. Since the discovery of mirror neurons (MNs) in the ventral premotor cortex, it has been assumed that their activation was conditional upon the presentation of biological rather than nonbiological motion stimuli, supporting a form of direct visuomotor matching. Nonetheless, nonbiological observed movements have rarely been used as control stimuli to evaluate visual specificity, thereby leaving the issue of similarity among neural codes for executed actions and biological or nonbiological observed movements unresolved. Here, we addressed this issue by recording from two nodes of the AON that are attracting increasing interest, namely the ventro-rostral part of the dorsal premotor area F2 and the mesial pre-supplementary motor area F6 of macaques while they 1) executed a reaching-grasping task, 2) observed an experimenter performing the task, and 3) observed a nonbiological effector moving in the same context. Our findings revealed stronger neuronal responses to the observation of biological than nonbiological movement, but biological and nonbiological visual stimuli produced highly similar neural dynamics and relied on largely shared neural codes, which in turn remarkably differed from those associated with executed actions. These results indicate that, in highly familiar contexts, visuo-motor remapping processes in premotor areas hosting MNs are more complex and flexible than predicted by a direct visuomotor matching hypothesis.


2021 ◽  
pp. 102214
Author(s):  
Giovanni Pezzulo ◽  
Francesco Donnarumma ◽  
Simone Ferrari-Toniolo ◽  
Paul Cisek ◽  
Alexandra Battaglia-Mayer

2020 ◽  
Vol 123 (3) ◽  
pp. 927-935
Author(s):  
David Thura ◽  
Paul Cisek

Humans and other animals are faced with decisions about actions on a daily basis. These typically include a period of deliberation that ends with the commitment to a choice, which then leads to the overt expression of that choice through action. Previous studies with monkeys have demonstrated that neural activity in sensorimotor areas correlates with the deliberation process and reflects the moment of commitment before movement initiation, but the causal roles of these regions are challenging to establish. Here, we tested whether dorsal premotor (PMd) and primary motor cortex (M1) are causally involved in the volitional commitment to a reaching choice. We found that brief subthreshold microstimulation in PMd or M1 delayed commitment to an action but not the initiation of the action itself. Importantly, microstimulation only had a significant effect when it was delivered close to and before commitment time. These results are consistent with the proposal that PMd and M1 participate in the commitment process, which occurs when a critical firing rate difference is reached between cells voting for the selected option and those voting for the competing one. NEW & NOTEWORTHY The neural substrates of decisions between actions are typically investigated by correlating neural activity and subjects’ decision behavior, but this does not establish causality. In a reaching decision task, we demonstrate that subthreshold microstimulation of the monkey dorsal premotor cortex or primary motor cortex delays the deliberation duration if applied shortly before choice commitment. This result suggests a causal role of the sensorimotor cortex in the determination of decisions between actions.


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