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

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)

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.


Author(s):  
Donald D. Samulack ◽  
Robert S. Waters ◽  
Robert W. Dykes ◽  
Patricia A. McKinley

ABSTRACT:Intracortical microstimulation (ICMS) was used to map the primary motor cortex of four adult female baboons, anesthetized with a mixture of halothane and nitrous oxide and supplemented with sodium pentobarbital. The sequence of observed muscle contractions in response to ICMS provided evidence of an orderly mototopic representation of the tongue, face, hand, forearm and upper body. A zone of cortex unresponsive to microstimulation was consistently observed at the border between the face and hand representation of the mototopic map. This zone was observed in all four animals and was consistent over time. Repeated confirmations of the unresponsive nature of these regions were obtained both early and late in the same experiment. No motor-unit responses or muscle contractions were detected by electromyographic (EMG) recording during stimulation of the unresponsive zones. The absence of both visually observed and EMG-recorded contractions and the fact that muscle contractions could be elicited from adjacent regions of cortex with ICMS as low as 1-5 μA provide compelling evidence that the finding reflects a true physiological condition rather than an experimental artifact.


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.


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.


1999 ◽  
Vol 82 (3) ◽  
pp. 1529-1541 ◽  
Author(s):  
Ruth E. Martin ◽  
Pentti Kemppainen ◽  
Yuji Masuda ◽  
Dongyuan Yao ◽  
Gregory M. Murray ◽  
...  

Although the cerebral cortex has been implicated in the control of swallowing, the output organization of the cortical swallowing representation, and features of cortically evoked swallowing, remain unclear. The present study defined the output features of the primate “cortical swallowing representation” with intracortical microstimulation (ICMS) applied within the lateral sensorimotor cortex. In four hemispheres of two awake monkeys, microelectrode penetrations were made at ≤1-mm intervals, initially within the face primary motor cortex (face-MI), and subsequently within the cortical regions immediately rostral, lateral, and caudal to MI. Two ICMS pulse trains [35-ms train, 0.2-ms pulses at 333 Hz, ≤30 μA (short train stimulus, T/S); 3- to 4-s train, 0.2-ms pulses at 50 Hz, ≤60 μA (continuous stimulus, C/S)] were applied at ≤500-μm intervals along each microelectrode penetration to a depth of 8–10 mm, and electromyographic (EMG) activity was recorded simultaneously from various orofacial and laryngeal muscles. Evoked orofacial movements, including swallowing, were verified by EMG analysis, and T/S and C/S movement thresholds were determined. Effects of varying ICMS intensity on swallow-related EMG properties were examined by applying suprathreshold C/S at selected intracortical sites. EMG patterns of swallows evoked from various cortical regions were compared with those of natural swallows recorded as the monkeys swallowed liquid and solid material. Results indicated that swallowing was evoked by C/S at ∼20% of 1,569 intracortical sites where ICMS elicited an orofacial motor response in both hemispheres of the two monkeys, typically at C/S intensities ≤30 μA. In contrast, swallowing was not evoked by T/S in either monkey. Swallowing was evoked from four cortical regions: the ICMS-defined face-MI, the face primary somatosensory cortex (face-SI), the region lateral and anterior to face-MI corresponding to the cortical masticatory area (CMA), and an area >5 mm deep to the cortical surface corresponding to both the white matter underlying the CMA and the frontal operculum; EMG patterns of swallows elicited from these four cortical regions showed some statistically significant differences. Whereas swallowing only was evoked at some sites, particularly within the deep cortical area, swallowing was more frequently evoked together with other orofacial responses including rhythmic jaw movements. Increasing ICMS intensity increased the magnitude, and decreased the latency, of the swallow-related EMG burst in the genioglossus muscle at some sites. These findings suggest that a number of distinct cortical foci may participate in the initiation and modulation of the swallowing synergy as well as in integrating the swallow within the masticatory sequence.


2005 ◽  
Vol 94 (4) ◽  
pp. 2353-2378 ◽  
Author(s):  
Lauren E. Sergio ◽  
Catherine Hamel-Pâquet ◽  
John F. Kalaska

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.


1992 ◽  
Vol 67 (3) ◽  
pp. 759-774 ◽  
Author(s):  
G. M. Murray ◽  
B. J. Sessle

1. The previous paper has described in detail the input and output features of single neurons located at sites within primate face motor cortex from which intracortical microstimulation (ICMS, less than or equal to 20 microA) evoked tongue movements at the lowest threshold ("tongue-MI" sites); for comparative purposes, we also reported on the input and output features of a smaller number of neurons recorded at sites from which ICMS could evoke jaw movements ("jaw-MI" sites), facial movements ("face-MI" sites), or, at a few sites, tongue movements and, at the same threshold intensity, either a jaw movement or a facial movement. 2. Our findings of an extensive and diverse representation of sites within face motor cortex of monkeys for the generation of elemental components of tongue movement, and the relatively few sites from which jaw-closing movements could be evoked, were consistent with our recent observations that reversible, cooling-induced inactivation of the face motor cortex severely impaired the performance by monkeys of a tongue-protrusion task but had only relatively minor effects on the performance of a biting task. In an attempt to establish a neuronal correlate for these different behavioral relations, the present study has documented the task-related activities of those single neurons that were characterized in the previous paper in terms of afferent input and ICMS-defined output features. 3. Each task required the development and maintenance by each monkey of a fixed force level for a minimum period of time to obtain a fruit-juice reward. During one or both of these tasks, we characterized the activities of 231 single face motor cortical neurons that were located at the above-mentioned ICMS-defined sites. Neurons were said to be related to a particular task if they showed statistically significant differences in firing rates during the task in comparison with a control pretrial period (PTP). 4. In tongue-MI, there was a significantly higher proportion of neurons (63% of 156 neurons tested) that were related to the tongue-protrusion task than to the biting task (15% of 65). However, in jaw-MI the proportion of neurons that were biting task-related (63% of 19) was significantly higher than the proportion related to the tongue-protrusion task (11% of 9); the proportion of biting task-related neurons at ICMS-defined jaw-closing sites was also higher than that at jaw-opening sites.(ABSTRACT TRUNCATED AT 400 WORDS)


2017 ◽  
Vol 122 (6) ◽  
pp. 1494-1503 ◽  
Author(s):  
Yasunori Abe ◽  
Chiho Kato ◽  
Karin Harumi Uchima Koecklin ◽  
Hidemasa Okihara ◽  
Takayoshi Ishida ◽  
...  

Postnatal growth is influenced by genetic and environmental factors. Nasal obstruction during growth alters the electromyographic activity of orofacial muscles. The facial primary motor area represents muscles of the tongue and jaw, which are essential in regulating orofacial motor functions, including chewing and jaw opening. This study aimed to evaluate the effect of chronic unilateral nasal obstruction during growth on the motor representations within the face primary motor cortex (M1). Seventy-two 6-day-old male Wistar rats were randomly divided into control ( n = 36) and experimental ( n = 36) groups. Rats in the experimental group underwent unilateral nasal obstruction after cauterization of the external nostril at 8 days of age. Intracortical microstimulation (ICMS) mapping was performed when the rats were 5, 7, 9, and 11 wk old in control and experimental groups ( n = 9 per group per time point). Repeated-measures multivariate ANOVA was used for intergroup and intragroup statistical comparisons. In the control and experimental groups, the total number of positive ICMS sites for the genioglossus and anterior digastric muscles was significantly higher at 5, 7, and 9 wk, but there was no significant difference between 9 and 11 wk of age. Moreover, the total number of positive ICMS sites was significantly smaller in the experimental group than in the control at each age. It is possible that nasal obstruction induced the initial changes in orofacial motor behavior in response to the altered respiratory pattern, which eventually contributed to face-M1 neuroplasticity. NEW & NOTEWORTHY Unilateral nasal obstruction in rats during growth periods induced changes in arterial oxygen saturation (SpO2) and altered development of the motor representation within the face primary cortex. Unilateral nasal obstruction occurring during growth periods may greatly affect not only respiratory function but also craniofacial function in rats. Nasal obstruction should be treated as soon as possible to avoid adverse effects on normal growth, development, and physiological functions.


Nature ◽  
2021 ◽  
Vol 598 (7879) ◽  
pp. 159-166
Author(s):  
Rodrigo Muñoz-Castañeda ◽  
Brian Zingg ◽  
Katherine S. Matho ◽  
Xiaoyin Chen ◽  
Quanxin Wang ◽  
...  

AbstractAn essential step toward understanding brain function is to establish a structural framework with cellular resolution on which multi-scale datasets spanning molecules, cells, circuits and systems can be integrated and interpreted1. Here, as part of the collaborative Brain Initiative Cell Census Network (BICCN), we derive a comprehensive cell type-based anatomical description of one exemplar brain structure, the mouse primary motor cortex, upper limb area (MOp-ul). Using genetic and viral labelling, barcoded anatomy resolved by sequencing, single-neuron reconstruction, whole-brain imaging and cloud-based neuroinformatics tools, we delineated the MOp-ul in 3D and refined its sublaminar organization. We defined around two dozen projection neuron types in the MOp-ul and derived an input–output wiring diagram, which will facilitate future analyses of motor control circuitry across molecular, cellular and system levels. This work provides a roadmap towards a comprehensive cellular-resolution description of mammalian brain architecture.


2002 ◽  
Vol 87 (5) ◽  
pp. 2531-2541 ◽  
Author(s):  
Dongyuan Yao ◽  
Kensuke Yamamura ◽  
Noriyuki Narita ◽  
Ruth E. Martin ◽  
Gregory M. Murray ◽  
...  

The present study was undertaken to determine the firing patterns and the mechanoreceptive field (RF) properties of neurons within the face primary motor cortex (face-MI) in relation to chewing and other orofacial movements in the awake monkey. Of a total of 107 face-MI neurons recorded, 73 of 74 tested had activity related to chewing and 47 of 66 neurons tested showed activity related to a trained tongue task. Of the 73 chewing-related neurons, 52 (71.2%) showed clear rhythmic activity during rhythmic chewing. A total of 32 (43.8%) also showed significant alterations in activity in relation to the swallowing of a solid food (apple) bolus. Many of the chewing-related neurons (81.8% of 55 tested) had an orofacial RF, which for most was on the tongue dorsum. Tongue protrusion was evoked by intracortical microstimulation (ICMS) at most (63.6%) of the recording sites where neurons fired during the rhythmic jaw-opening phase, whereas tongue retraction was evoked by ICMS at most (66.7%) sites at which the neurons firing during the rhythmic jaw-closing phase were recorded. Of the 47 task-related neurons, 21 of 22 (95.5%) examined also showed chewing-related activity and 29 (61.7%) demonstrated significant alteration in activity in relation to the swallowing of a juice reward. There were no significant differences in the peak firing frequency among neuronal activities related to chewing, swallowing, or the task. These findings provide further evidence that face-MI may play an important role not only in trained orofacial movements but also in chewing as well as swallowing, including the control of tongue and jaw movements that occur during the masticatory sequence.


Sign in / Sign up

Export Citation Format

Share Document