Representation of individual forelimb muscles in primary motor cortex

Stimulus-triggered averaging (StTA) of forelimb muscle electromyographic (EMG) activity was used to investigate individual forelimb muscle representation within the primary motor cortex (M1) of rhesus macaques with the objective of determining the extent of intra-areal somatotopic organization. Two monkeys were trained to perform a reach-to-grasp task requiring multijoint coordination of the forelimb. EMG activity was simultaneously recorded from 24 forelimb muscles including 5 shoulder, 7 elbow, 5 wrist, 5 digit, and 2 intrinsic hand muscles. Microstimulation (15 µA at 15 Hz) was delivered throughout the movement task and individual stimuli were used as triggers for generating StTAs of EMG activity. StTAs were used to map the cortical representations of individual forelimb muscles. As reported previously (Park et al. 2001), cortical maps revealed a central core of distal muscle (wrist, digit, and intrinsic hand) representation surrounded by a horseshoe-shaped proximal (shoulder and elbow) muscle representation. In the present study, we found that shoulder and elbow flexor muscles were predominantly represented in the lateral branch of the horseshoe whereas extensors were predominantly represented in the medial branch. Distal muscles were represented within the core distal forelimb representation and showed extensive overlap. For the first time, we also show maps of inhibitory output from motor cortex, which follow many of the same organizational features as the maps of excitatory output. NEW & NOTEWORTHY While the orderly representation of major body parts along the precentral gyrus has been known for decades, questions have been raised about the possible existence of additional more detailed aspects of somatotopy. In this study, we have investigated this question with respect to muscles of the arm and show consistent features of within-arm (intra-areal) somatotopic organization. For the first time we also show maps of how inhibitory output from motor cortex is organized.

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Properties of Primary Motor Cortex Output to Forelimb Muscles in Rhesus Macaques

Journal of Neurophysiology ◽

10.1152/jn.00649.2003 ◽

2004 ◽

Vol 92 (5) ◽

pp. 2968-2984 ◽

Cited By ~ 68

Author(s):

Michael C. Park ◽

Abderraouf Belhaj-Saïf ◽

Paul D. Cheney

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Rhesus Macaques ◽

Red Nucleus ◽

Macaque Monkey ◽

Emg Activity ◽

Reach To Grasp ◽

Distal Muscle ◽

Forelimb Muscles ◽

Multijoint Movements

Stimulus-triggered averaging (StTA) of electromyographic (EMG) activity from 24 simultaneously recorded forelimb muscles was used to investigate properties of primary motor cortex (M1) output in the macaque monkey. Two monkeys were trained to perform a reach-to-grasp task requiring multijoint coordination of the forelimb. EMG activity was recorded from 24 forelimb muscles including 5 shoulder, 7 elbow, 5 wrist, 5 digit, and 2 intrinsic hand muscles. Microstimulation (15 μA at 15 Hz) was delivered throughout the movement task. From 297 stimulation sites in M1, a total of 2,079 poststimulus effects (PStE) were obtained including 1,398 poststimulus facilitation (PStF) effects and 681 poststimulus suppression (PStS) effects. Of the PStF effects, 60% were in distal and 40% in proximal muscles; 43% were of extensors and 47% flexors. For PStS, the corresponding numbers were 55 and 45% and 36 and 55%, respectively. M1 output effects showed extensive cofacilitation of proximal and distal muscles (96 sites, 42%) including 47 sites that facilitated at least one shoulder, elbow, and distal muscle, 45 sites that facilitated an elbow muscle and a distal muscle, and 22 sites that facilitated at least one muscle at all joints. The muscle synergies represented by outputs from these sites may serve an important role in the production of coordinated, multijoint movements. M1 output effects showed many similarities with red nucleus output although red nucleus effects were generally weaker and showed a strong bias toward facilitation of extensor muscles and a greater tendency to facilitate synergies involving muscles at noncontiguous joints.

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Postnatal Development of the Motor Representation in Primary Motor Cortex

Journal of Neurophysiology ◽

10.1152/jn.2000.84.5.2582 ◽

2000 ◽

Vol 84 (5) ◽

pp. 2582-2594 ◽

Cited By ~ 51

Author(s):

Samit Chakrabarty ◽

John H. Martin

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Muscle Tone ◽

Stimulus Frequency ◽

Emg Activity ◽

Postnatal Life ◽

Motor Representation ◽

Somatotopic Organization ◽

Train Duration ◽

Elbow Movement

The purpose of this study was to examine when the muscles and joints of the forelimb become represented in primary motor cortex (M1) during postnatal life and how local representation patterns change. We examined these questions in cats that were anesthetized (45–90 days, n = 14; adults, n = 3) and awake ( n = 4; 52–86 days). We used intracortical microstimulation (45 ms duration train, 330 Hz, 0.2-ms balanced biphasic pulses, with a leading cathodic pulse; up to 100 μA). In young animals (less than day 70), we also used stimulus trains and pulses that could produce greater temporal summation (up to 200-ms train duration, down to 143-Hz stimulus frequency, up to 0.8-ms pulse width). Anesthetized animals were areflexic, and muscle tone was similar to that of the awake cats (i.e., relaxed, not weight or load bearing, with minimal resistance to passive stretch). We monitored the kinematic effects of microstimulation and changes in electromyographic (EMG) activity in forelimb muscles. There was an age-dependent reduction in the number of sites where microstimulation did not produce a motor effect (i.e., ineffective sites), from 95% in animals younger than 60 days to 33% between 81 and 90 days. In adults, 24% of sites were ineffective. Median current thresholds for evoking movements dropped from 79 μA in animals younger than day 60 to 38 and 28 μA in day 81–90 animals and adults, respectively. There was a proximal-to-distal development of the somatotopic organization of the motor map. Stimulation at the majority of sites in animals younger than day 71 produced shoulder and elbow movement. Wrist sites were first present by day 71, and digit sites by day 81. Sites at which multiple responses were evoked, between 1.0 and 1.5 times threshold, were present after day 71, and increased with age. A higher percentage of distal joints were co-represented with other joints, rather than being represented alone. We found that effective sites initially were scattered and new sites representing proximal and distal joints filled in the gaps between effective sites. During most of the period examined, development of the caudal M1 subregion lagged that of the rostral subregion (percent of effective sites; threshold currents), although these differences were minimal or absent in adults. Our results show that the M1 motor representation is absent at day 45 and, during the subsequent month, the motor map is constructed by progressively representing more distal forelimb joints.

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Constraints on Somatotopic Organization in the Primary Motor Cortex

Journal of Neurophysiology ◽

10.1152/jn.2001.86.5.2125 ◽

2001 ◽

Vol 86 (5) ◽

pp. 2125-2143 ◽

Cited By ~ 346

Author(s):

Marc H. Schieber

Keyword(s):

Motor Cortex ◽

20Th Century ◽

Primary Motor Cortex ◽

Body Parts ◽

Single Experiment ◽

Somatotopic Organization ◽

Point Representation ◽

The Face ◽

Middle Ring ◽

Point To Point

Since the 1870s, the primary motor cortex (M1) has been known to have a somatotopic organization, with different regions of cortex participating in control of face, arm, and leg movements. Through the middle of the 20th century, it seemed possible that the principle of somatotopic organization extended to the detailed representation of different body parts within each of the three major representations. The arm region of M1, for example, was thought to contain a well-ordered, point-to-point representation of the movements or muscles of the thumb, index, middle, ring, and little fingers, the wrist, elbow, and shoulder, as conveyed by the iconic homunculus and simiusculus. In the last quarter of the 20th century, however, experimental evidence has accumulated indicating that within-limb somatotopy in M1 is not spatially discrete nor sequentially ordered. Rather, beneath gradual somatotopic gradients of representation, the representations of different smaller body parts or muscles each are distributed widely within the face, arm, or leg representation, such that the representations of any two smaller parts overlap extensively. Appreciation of this underlying organization will be essential to further understanding of the contribution to control of movement made by M1. Because no single experiment disproves a well-ordered within-limb somatotopic organization in M1, here I review the accumulated evidence, using a framework of six major features that constrain the somatotopic organization of M1: convergence of output, divergence of output, horizontal interconnections, distributed activation, effects of lesions, and ability to reorganize. Review of the classic experiments that led to development of the homunculus and simiusculus shows that these data too were consistent with distributed within-limb somatotopy. I conclude with speculations on what the constrained somatotopy of M1 might tell us about its contribution to control of movement.

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Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

10.1101/457002 ◽

2018 ◽

Cited By ~ 1

Author(s):

Laurentius Huber ◽

Emily S. Finn ◽

Daniel A. Handwerker ◽

Marlene Bönstrup ◽

Daniel Glen ◽

...

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Functional Organization ◽

Large Body ◽

Body Parts ◽

Human Motor Cortex ◽

Somatotopic Organization ◽

Starting Point ◽

Motor Actions ◽

Hands And Feet

The human brain coordinates a wide variety of motor activities. On a large scale, the cortical motor system is topographically organized such that neighboring body parts are represented by neighboring brain areas. This homunculus-like somatotopic organization along the central sulcus has been observed using neuroimaging for large body parts such as the face, hands and feet. However, on a finer scale, invasive electrical stimulation studies show deviations from this somatotopic organization that suggest an organizing principle based on motor actions rather than body part moved. It has not been clear how the action-map organization principle of the motor cortex in the mesoscopic (sub-millimeter) regime integrates into a body map organization principle on a macroscopic scale (cm). Here we developed and applied advanced mesoscopic (sub-millimeter) fMRI and analysis methodology to non-invasively investigate the functional organization topography across columnar and laminar structures in humans. We find that individual fingers have multiple mirrored representations in the primary motor cortex depending on the movements they are involved in. We find that individual digits have cortical representations up to 3 mm apart from each other arranged in a column-like fashion. These representations are differentially engaged depending on whether the digits’ muscles are used for different motor actions such as flexion movements like grasping a ball or retraction movements like releasing a ball. This research provides a starting point for noninvasive investigation of mesoscale topography across layers and columns of the human cortex and bridges the gap between invasive electrophysiological investigations and large coverage non-invasive neuroimaging.

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Motor Cortical Activity During Drawing Movements: Population Representation During Spiral Tracing

Journal of Neurophysiology ◽

10.1152/jn.1999.82.5.2693 ◽

1999 ◽

Vol 82 (5) ◽

pp. 2693-2704 ◽

Cited By ~ 114

Author(s):

Daniel W. Moran ◽

Andrew B. Schwartz

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Prediction Interval ◽

Premotor Cortex ◽

Cortical Activity ◽

Simultaneous Action ◽

Emg Activity ◽

Radius Of Curvature ◽

Time Interval ◽

Population Vector

Monkeys traced spirals on a planar surface as unitary activity was recorded from either premotor or primary motor cortex. Using the population vector algorithm, the hand's trajectory could be accurately visualized with the cortical activity throughout the task. The time interval between this prediction and the corresponding movement varied linearly with the instantaneous radius of curvature; the prediction interval was longer when the path of the finger was more curved (smaller radius). The intervals in the premotor cortex fell into two groups, whereas those in the primary motor cortex formed a single group. This suggests that the change in prediction interval is a property of a single population in primary motor cortex, with the possibility that this outcome is due to the different properties generated by the simultaneous action of separate subpopulations in premotor cortex. Electromyographic (EMG) activity and joint kinematics were also measured in this task. These parameters varied harmonically throughout the task with many of the same characteristics as those of single cortical cells. Neither the lags between joint-angular velocities and hand velocity nor the lags between EMG and hand velocity could explain the changes in prediction interval between cortical activity and hand velocity. The simple spatial and temporal relationship between cortical activity and finger trajectory suggests that the figural aspects of this task are major components of cortical activity.

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Effective intracortical microstimulation parameters applied to primary motor cortex for evoking forelimb movements to stable spatial end points

Journal of Neurophysiology ◽

10.1152/jn.00172.2012 ◽

2013 ◽

Vol 110 (5) ◽

pp. 1180-1189 ◽

Cited By ~ 14

Author(s):

Gustaf M. Van Acker ◽

Sommer L. Amundsen ◽

William G. Messamore ◽

Hongyu Y. Zhang ◽

Carl W. Luchies ◽

...

Keyword(s):

Motor Cortex ◽

Large Scale ◽

Primary Motor Cortex ◽

Emg Activity ◽

Intracortical Microstimulation ◽

End Points ◽

End Point ◽

Motor Effects ◽

Forelimb Movements ◽

Stimulation Of

High-frequency, long-duration intracortical microstimulation (HFLD-ICMS) applied to motor cortex is recognized as a useful and informative method for corticomotor mapping by evoking natural-appearing movements of the limb to consistent stable end-point positions. An important feature of these movements is that stimulation of a specific site in motor cortex evokes movement to the same spatial end point regardless of the starting position of the limb. The goal of this study was to delineate effective stimulus parameters for evoking forelimb movements to stable spatial end points from HFLD-ICMS applied to primary motor cortex (M1) in awake monkeys. We investigated stimulation of M1 as combinations of frequency (30–400 Hz), amplitude (30–200 μA), and duration (0.5–2 s) while concurrently recording electromyographic (EMG) activity from 24 forelimb muscles and movement kinematics with a motion capture system. Our results suggest a range of parameters (80–140 Hz, 80–140 μA, and 1,000-ms train duration) that are effective and safe for evoking forelimb translocation with subsequent stabilization at a spatial end point. The mean time for stimulation to elicit successful movement of the forelimb to a stable spatial end point was 475.8 ± 170.9 ms. Median successful frequency and amplitude were 110 Hz and 110 μA, respectively. Attenuated parameters resulted in inconsistent, truncated, or undetectable movements, while intensified parameters yielded no change to movement end points and increased potential for large-scale physiological spread and adverse focal motor effects. Establishing cortical stimulation parameters yielding consistent forelimb movements to stable spatial end points forms the basis for a systematic and comprehensive mapping of M1 in terms of evoked movements and associated muscle synergies. Additionally, the results increase our understanding of how the central nervous system may encode movement.

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Organization of the primate face motor cortex as revealed by intracortical microstimulation and electrophysiological identification of afferent inputs and corticobulbar projections

Journal of Neurophysiology ◽

10.1152/jn.1988.59.3.796 ◽

1988 ◽

Vol 59 (3) ◽

pp. 796-818 ◽

Cited By ~ 106

Author(s):

C. S. Huang ◽

M. A. Sirisko ◽

H. Hiraba ◽

G. M. Murray ◽

B. J. Sessle

Keyword(s):

Motor Cortex ◽

Single Neuron ◽

Primary Motor Cortex ◽

General Pattern ◽

Emg Activity ◽

Projection Neurons ◽

Intracortical Microstimulation ◽

Facial Musculature ◽

The Face ◽

Afferent Inputs

1. The technique of intracortical microstimulation (ICMS), supplemented by single-neuron recording, was used to carry out an extensive mapping of the face primary motor cortex. The ICMS study involved a total of 969 microelectrode penetrations carried out in 10 unanesthetized monkeys (Macaca fascicularis). 2. Monitoring of ICMS-evoked movements and associated electromyographic (EMG) activity revealed a general pattern of motor cortical organization. This was characterized by a representation of the facial musculature, which partially enclosed and overlapped the rostral, medial, and caudal borders of the more laterally located cortical regions representing the jaw and tongue musculatures. Responses were evoked at ICMS thresholds as low as 1 microA, and the latency of the suprathreshold EMG responses ranged from 10 to 45 ms. 3. Although contralateral movements predominated, a representation of ipsilateral movements was found, which was much more extensive than previously reported and which was intermingled with the contralateral representations in the anterior face motor cortex. 4. In examining the fine organizational pattern of the representations, we found clear evidence for multiple representation of a particular muscle, thus supporting other investigations of the motor cortex, which indicate that multiple, yet discrete, efferent microzones represent an essential organizational principle of the motor cortex. 5. The close interrelationship of the representations of all three muscle groups, as well as the presence of a considerable ipsilateral representation, may allow for the necessary integration of unilateral or bilateral activities of the numerous face, jaw, and tongue muscles, which is a feature of many of the movement patterns in which these various muscles participate. 6. In six of these same animals, plus an additional two animals, single-neuron recordings were made in the motor and adjacent sensory cortices in the anesthetized state. These neurons were electrophysiologically identified as corticobulbar projection neurons or as nonprojection neurons responsive to superficial or deep orofacial afferent inputs. The rostral, medial, lateral, and caudal borders of the face motor cortex were delineated with greater definition by ICMS and these electrophysiological procedures than by cytoarchitectonic features alone. We noted that there was an approximate fit in area 4 between the extent of projection neurons and field potentials anti-dromically evoked from the brain stem and the extent of positive ICMS sites.(ABSTRACT TRUNCATED AT 400 WORDS)

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Sequential activation of neurons in primate motor cortex during unrestrained forelimb movement

Journal of Neurophysiology ◽

10.1152/jn.1985.53.2.435 ◽

1985 ◽

Vol 53 (2) ◽

pp. 435-445 ◽

Cited By ~ 36

Author(s):

J. T. Murphy ◽

Y. C. Wong ◽

H. C. Kwan

Keyword(s):

Motor Cortex ◽

Emg Activity ◽

Zone Model ◽

Somatosensory Stimulation ◽

Reaching Movement ◽

Sequential Activation ◽

Forelimb Muscles ◽

Muscle Groups ◽

Forelimb Movement ◽

Discharge Patterns

We trained monkeys to perform an unrestrained, reaching movement of the arm. Electromyogram (EMG) recordings of forelimb muscles revealed sequential activation, proximal to distal, of muscle groups involved in the task. The delay in onset of EMG activity between proximal (shoulder and elbow) and distal (wrist and finger) muscles was approximately 60 ms. We identified the neurons in the forelimb area of the contralateral motor cortex as controlling particular joints by previously defined criteria involving responses to somatosensory stimulation and effects of intracortical microstimulation. Many cells discharged prior to the onset of EMG activity acting on the appropriate joint, whereas others began firing at a later phase of the movement. The population of all proximal cells altered discharge patterns approximately 60 ms earlier than the population of distal cells. A small percentage of cells showed an initial inhibitory change in discharge frequency, and this inhibition typically occurred prior to the excitatory changes seen in the majority of cells. The results are discussed in terms of the "nested-zone" model of the forelimb motor cortex. The data support one of the predictions of this model, namely that discharges of identified cells within the cortical zones are causally related to voluntary movement at appropriate forelimb joints.

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Motor Cortex Neural Correlates of Output Kinematics and Kinetics During Isometric-Force and Arm-Reaching Tasks

Journal of Neurophysiology ◽

10.1152/jn.00989.2004 ◽

2005 ◽

Vol 94 (4) ◽

pp. 2353-2378 ◽

Cited By ~ 148

Author(s):

Lauren E. Sergio ◽

Catherine Hamel-Pâquet ◽

John F. Kalaska

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Isometric Force ◽

Arm Movements ◽

Population Level ◽

Emg Activity ◽

Hand Motion ◽

Arm Reaching ◽

Direction Of Movement ◽

Isometric Forces

We recorded the activity of 132 proximal-arm-related neurons in caudal primary motor cortex (M1) of two monkeys while they generated either isometric forces against a rigid handle or arm movements with a heavy movable handle, in the same eight directions in a horizontal plane. The isometric forces increased in monotonic fashion in the direction of the force target. The forces exerted against the handle in the movement task were more complex, including an initial accelerating force in the direction of movement followed by a transient decelerating force opposite to the direction of movement as the hand approached the target. EMG activity of proximal-arm muscles reflected the difference in task dynamics, showing directional ramplike activity changes in the isometric task and reciprocally tuned “triphasic” patterns in the movement task. The apparent instantaneous directionality of muscle activity, when expressed in hand-centered spatial coordinates, remained relatively stable during the isometric ramps but often showed a large transient shift during deceleration of the arm movements. Single-neuron and population-level activity in M1 showed similar task-dependent changes in temporal pattern and instantaneous directionality. The momentary dissociation of the directionality of neuronal discharge and movement kinematics during deceleration indicated that the activity of many arm-related M1 neurons is not coupled only to the direction and speed of hand motion. These results also demonstrate that population-level signals reflecting the dynamics of motor tasks and of interactions with objects in the environment are available in caudal M1. This task-dynamics signal could greatly enhance the performance capabilities of neuroprosthetic controllers.

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