Neuronal Activity Patterns in Primate Primary Motor Cortex Related to Trained or Semiautomatic Jaw and Tongue Movements

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.

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)


1992 ◽  
Vol 67 (3) ◽  
pp. 747-758 ◽  
Author(s):  
G. M. Murray ◽  
B. J. Sessle

1. We have recently demonstrated that reversible, cooling-induced inactivation of the face motor cortex results in a severe impairment in the ability of monkeys (Macaca fascicularis) to perform a tongue-protrusion task but produces only relatively minor effects on the performance of a biting task by the same monkeys. To establish a neuronal correlate for these different behavioral relations, the present study has detailed the afferent input and intracortical microstimulation (ICMS)-defined output features of a population of face motor cortical neurons, and in a subsequent study we have documented the activities of the same population of neurons during the performance of the tongue-protrusion and biting tasks. 2. Of the 231 single neurons recorded within the face motor cortex, 163 were located at sites from which ICMS (less than or equal to 20 microA) could evoke tongue movements (i.e., "tongue-MI" sites) at the lowest threshold for eliciting orofacial movements. The remainder were located at sites from which ICMS evoked jaw movements ("jaw-MI" sites), face 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. 3. We confirmed the general organizational features of the face motor cortex that have been defined in previous studies, but we documented in detail the organizational features for tongue-MI. Thus we found that tongue movements were well represented, whereas jaw-closing movements were poorly represented; the representations for face, jaw, and tongue movements were overlapped; the same ICMS-evoked tongue movement could be multiply represented within tongue-MI; tongue-MI was characterized by a prominent input from superficial mechanosensory afferents, whereas there was little evidence for deep input; a close spatial match was found between ICMS-defined motor output and somatosensory afferent input for tongue-MI. 4. A variety of tongue movements could be evoked by ICMS at tongue-MI sites and were categorized into protrusion, retrusion, laterally directed, and other types of tongue movement. Low-threshold (i.e., less than or equal to 5 microA) ICMS-defined tongue-MI sites, which were considered to represent "efferent zones" projecting relatively directly to motoneurons, were reconstructed three dimensionally to provide insights into the spatial organization of tongue-MI. Examples of each of the four low-threshold efferent-zone categories were usually found throughout the ICMS-defined tongue-MI without any apparent preferential distribution. Furthermore, different low-threshold efferent-zone categories had close spatial relationships to each other in cortex.(ABSTRACT TRUNCATED AT 400 WORDS)


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 78 (3) ◽  
pp. 1516-1530 ◽  
Author(s):  
Ruth E. Martin ◽  
Gregory M. Murray ◽  
Pentti Kemppainen ◽  
Yuji Masuda ◽  
Barry J. Sessle

Martin, Ruth E., Gregory M. Murray, Pentti Kemppainen, Yuji Masuda, and Barry J. Sessle. Functional properties of neurons in the primate tongue primary motor cortex during swallowing. J. Neurophysiol. 78: 1516–1530, 1997. Recent studies conducted in our laboratory have suggested that the tongue primary motor cortex (i.e., tongue-MI) plays a critical role in the control of voluntary tongue movements in the primate. However, the possible involvement of tongue-MI in semiautomatic tongue movements, such as those in swallowing, remains unkown. Therefore the present study was undertakein in attempts to address whether tongue-MI plays a role in the semiautomatic tongue movements produced during swallowing. Extracellular single neuron recordings were obtained from tongue-MI, defined by intracortical microstimulation (ICMS), in two awake monkeys as they performed three types of swallowing (swallowing of a juice reward after successful tongue task performance, nontask-related swallowing of a liquid bolus, and nontask-related swallowing of a solid bolus) as well as a trained tongue-protrusion task. Electromyographic activity was recorded simultaneously from various orofacial and laryngeal muscles. In addition, the afferent input to each tongue-MI neuron and ICMS-evoked motor output characteristics at each neuronal recording site were determined. Neurons were considered to show swallow and/or tongue-protrusion task-related activity if a statistically significant difference in firing rate was seen in association with these behaviors compared with that observed during a control pretrial period. Of a total of 80 neurons recorded along 40 microelectrode penetrations in the ICMS-defined tongue-MI, 69% showed significant alterations of activity in relation to the swallowing of a juice reward, whereas 66% exhibited significant modulations of firing in association with performance of the trained tongue-protrusion task. Moreover, 48% showed significant alterations of firing in relation to both swallowing and the tongue-protrusion task. These findings suggest that the region of cortex involved in swallowing includes MI and that tongue-MI may play a role in the regulation of semiautomatic tongue movement, in addition to trained motor behavior. Swallow-related tongue-MI neurons exhibited a variety of swallow-related activity patterns and were distributed throughout the ICMS-defined tongue-MI at sites where ICMS evoked a variety of types of tongue movements. These findings are consistent with the view that multiple efferent zones for the production of tongue movements are activated in swallowing. Many swallow-related tongue-MI neurons had an orofacial mechanoreceptive field, particularly on the tongue dorsum, supporting the view that afferent inputs may be involved in the regulation of the swallowing synergy.


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.


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.


2007 ◽  
Vol 97 (1) ◽  
pp. 70-82 ◽  
Author(s):  
Marc H. Schieber ◽  
Gil Rivlis

Primary motor cortex (M1) neurons traditionally have been viewed as “upper motor neurons” that directly drive spinal motoneuron pools, particularly during finger movements. We used spike-triggered averages (SpikeTAs) of electromyographic (EMG) activity to select M1 neurons whose spikes signaled the arrival of input in motoneuron pools, and examined the degree of similarity between the activity patterns of these M1 neurons and their target muscles during 12 individuated finger and wrist movements. Neuron–EMG similarity generally was low. Similarity was unrelated to the strength of the SpikeTA effect, to whether the effect was pure versus synchrony, or to the number of muscles influenced by the neuron. Nevertheless, the sum of M1 neuron activity patterns, each weighted by the sign and strength of its SpikeTA effect, could be more similar to the EMG than the average similarity of individual neurons. Significant correlations between the weighted sum of M1 neuron activity patterns and EMG were obtained in six of 17 muscles, but showed R2 values ranging from only 0.26 to 0.42. These observations suggest that additional factors—including inputs from sources other than M1 and nonlinear summation of inputs to motoneuron pools—also contributed substantially to EMG activity patterns. Furthermore, although each of these M1 neurons produced SpikeTA effects with a significant peak or trough 6–16 ms after the triggering spike, shifting the weighted sum of neuron activity to lead the EMG by 40–60 ms increased their similarity, suggesting that the influence of M1 neurons that produce SpikeTA effects includes substantial synaptic integration that in part may reach the motoneuron pools over less-direct pathways.


2015 ◽  
Vol 523 (16) ◽  
pp. 2372-2389 ◽  
Author(s):  
Limor Avivi-Arber ◽  
Jye-Chang Lee ◽  
Mandeep Sood ◽  
Flavia Lakschevitz ◽  
Michelle Fung ◽  
...  

2020 ◽  
Vol 2020 ◽  
pp. 1-8
Author(s):  
Weiqin Peng ◽  
Tiange Yang ◽  
Jiawei Yuan ◽  
Jianpeng Huang ◽  
Jianhua Liu

Somatosensory stimulation can effectively induce plasticity in the motor cortex representation of the stimulated body part. Specific interactions have been reported between different representations within the primary motor cortex. However, studies evaluating somatosensory stimulation-induced plasticity between different representations within the primary motor cortex are sparse. The purpose of this study was to investigate the effect of somatosensory stimulation on the modulation of plasticity between different representations within the primary motor cortex. Twelve healthy volunteers received both electroacupuncture (EA) and sham EA at the TE5 acupoint (located on the forearm). Plasticity changes in different representations, including the map volume, map area, and centre of gravity (COG) were evaluated by transcranial magnetic stimulation (TMS) before and after the intervention. EA significantly increased the map volume of the forearm and hand representations compared to those of sham EA and significantly reduced the map volume of the face representation compared to that before EA. No significant change was found in the map volume of the upper arm and leg representations after EA, and likewise, no significant changes in map area and COG were observed. These results suggest that EA functions as a form of somatosensory stimulation to effectively induce plasticity between different representations within the primary motor cortex, which may be related to the extensive horizontal intrinsic connectivity between different representations. The cortical plasticity induced by somatosensory stimulation might be purposefully used to modulate human cortical function.


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