scholarly journals Muscle synergies obtained from comprehensive mapping of the primary motor cortex forelimb representation using high-frequency, long-duration ICMS

2017 ◽  
Vol 118 (1) ◽  
pp. 455-470 ◽  
Author(s):  
Sommer L. Amundsen Huffmaster ◽  
Gustaf M. Van Acker ◽  
Carl W. Luchies ◽  
Paul D. Cheney

Simplifying neuromuscular control for movement has previously been explored by extracting muscle synergies from voluntary movement electromyography (EMG) patterns. The purpose of this study was to investigate muscle synergies represented in EMG recordings associated with direct electrical stimulation of single sites in primary motor cortex (M1). We applied single-electrode high-frequency, long-duration intracortical microstimulation (HFLD-ICMS) to the forelimb region of M1 in two rhesus macaques using parameters previously found to produce forelimb movements to stable spatial end points (90–150 Hz, 90–150 μA, 1,000-ms stimulus train lengths). To develop a comprehensive representation of cortical output, stimulation was applied systematically across the full extent of M1. We recorded EMG activity from 24 forelimb muscles together with movement kinematics. Nonnegative matrix factorization (NMF) was applied to the mean stimulus-evoked EMG, and the weighting coefficients associated with each synergy were mapped to the cortical location of the stimulating electrode. Synergies were found for three data sets including 1) all stimulated sites in the cortex, 2) a subset of sites that produced stable movement end points, and 3) EMG activity associated with voluntary reaching. Two or three synergies accounted for 90% of the overall variation in voluntary movement EMG whereas four or five synergies were needed for HFLD-ICMS-evoked EMG data sets. Maps of the weighting coefficients from the full HFLD-ICMS data set show limited regional areas of higher activation for particular synergies. Our results demonstrate fundamental NMF-based muscle synergies in the collective M1 output, but whether and how the central nervous system might coordinate movements using these synergies remains unclear. NEW & NOTEWORTHY While muscle synergies have been investigated in various muscle activity sets, it is unclear whether and how synergies may be organized in the cortex. We have investigated muscle synergies resulting from high-frequency, long-duration intracortical microstimulation (HFLD-ICMS) applied throughout M1. We compared HFLD-ICMS synergies to synergies from voluntary movement. While synergies can be identified from M1 stimulation, they are not clearly related to voluntary movement synergies and do not show an orderly topographic organization across M1.

2013 ◽  
Vol 110 (5) ◽  
pp. 1180-1189 ◽  
Author(s):  
Gustaf M. Van Acker ◽  
Sommer L. Amundsen ◽  
William G. Messamore ◽  
Hongyu Y. Zhang ◽  
Carl W. Luchies ◽  
...  

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.


1988 ◽  
Vol 59 (3) ◽  
pp. 796-818 ◽  
Author(s):  
C. S. Huang ◽  
M. A. Sirisko ◽  
H. Hiraba ◽  
G. M. Murray ◽  
B. J. Sessle

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)


1997 ◽  
Vol 77 (5) ◽  
pp. 2446-2465 ◽  
Author(s):  
Gail L. Widener ◽  
Paul D. Cheney

Widener, Gail L. and Paul D. Cheney. Effects on muscle activity from microstimuli applied to somatosensory and motor cortex during voluntary movement in the monkey. J. Neurophysiol. 77: 2446–2465, 1997. It is well known that electrical stimulation of primary somatosensory cortex (SI) evokes movements that resemble those evoked from primary motor cortex. These findings have led to the concept that SI may possess motor capabilities paralleling those of motor cortex and speculation that SI could function as a robust relay mediating motor responses from central and peripheral inputs. The purpose of this study was to rigorously examine the motor output capabilities of SI areas with the use of the techniques of spike- and stimulus-triggered averaging of electromyographic (EMG) activity in awake monkeys. Unit recordings were obtained from primary motor cortex and SI areas 3a, 3b, 1, and 2 in three rhesus monkeys. Spike-triggered averaging was used to assess the output linkage between individual cells and motoneurons of the recorded muscles. Cells in motor cortex producing postspike facilitation (PSpF) in spike-triggered averages of rectified EMG activity were designated corticomotoneuronal (CM) cells. Motor output efficacy was also assessed by applying stimuli through the microelectrode and computing stimulus-triggered averages of rectified EMG activity. One hundred seventy-one sites in motor cortex and 68 sites in SI were characterized functionally and tested for motor output effects on muscle activity. The incidence, character, and magnitude of motor output effects from SI areas were in sharp contrast to effects from CM cell sites in primary motor cortex. Of 68 SI cells tested with spike-triggered averaging, only one area 3a cell produced significant PSpF in spike-triggered averages of EMG activity. In comparison, 20 of 171 (12%) motor cortex cells tested produced significant postspike effects. Single-pulse intracortical microstimulation produced effects at all CM cell sites in motor cortex but at only 14% of SI sites. The large fraction of SI effects that was inhibitory represented yet another marked difference between CM cell sites in motor cortex and SI sites (25% vs 93%). The fact that motor output effects from SI were frequently absent or very weak and predominantly inhibitory emphasizes the differing motor capabilities of SI compared with primary motor cortex.


1999 ◽  
Vol 82 (5) ◽  
pp. 2693-2704 ◽  
Author(s):  
Daniel W. Moran ◽  
Andrew B. Schwartz

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.


NeuroImage ◽  
2008 ◽  
Vol 42 (1) ◽  
pp. 332-342 ◽  
Author(s):  
Douglas Cheyne ◽  
Sonya Bells ◽  
Paul Ferrari ◽  
William Gaetz ◽  
Andreea C. Bostan

Author(s):  
Robert Chen ◽  
Leonardo G. Cohen ◽  
Mark Hallett

ABSTRACT:The ipsilateral primary motor cortex (M1) plays a role in voluntary movement. In our studies, we used repetitive transcranial magnetic stimulation (rTMS) to study the effects of transient disruption of the ipsilateral M1 on the performance of finger sequences in right-handed normal subjects. Stimulation of the M1 ipsilateral to the movement induced timing errors in both simple and complex sequences performed with either hand, but with complex sequences, the effects were more pronounced with the left-sided stimulation. Recent studies in both animals and humans have confirmed the traditional view that ipsilateral projections from M1 to the upper limb are mainly directed to truncal and proximal muscles, with little evidence for direct connections to distal muscles. The ipsilateral motor pathway appears to be an important mechanism for functional recovery after focal brain injury during infancy, but its role in functional recovery for older children and adults has not yet been clearly demonstrated. There is increasing evidence from studies using different methodologies such as rTMS, functional imaging and movement-related cortical potentials, that M1 is involved in ipsilateral hand movements, with greater involvement in more complex tasks and the left hemisphere playing a greater role than the right.


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