scholarly journals Comparing Cerebellar and Motor Cortical Activity in Reaching and Grasping

Author(s):  
M. Smith Allan ◽  
Dugas Clause ◽  
Fortier Pierre ◽  
Kalasha John ◽  
Picard Nathalie

ABSTRACT:The activity of single cells in the cerebellar and motor cortex of awake monkeys was recorded during separate studies of whole-arm reaching movements and during the application of force-pulse perturbations to handheld objects. Two general observations about the contribution of the cerebellum to the control of movement emerge from the data. The first, derived from the study of whole arm reaching, suggests that although both the motor cortex and cerebellum generate a signal related to movement direction, the cerebellar signal is less precise and varies from trial to trial even when the movement kinematics remain unchanged. The second observation, derived from the study of predictable perturbations of a hand-held object, indicates that cerebellar cortical neurons better reflect preparatory motor strategies formed from the anticipation of cutaneous and proprioceptive stimuli acquired by previous experience. In spite of strong relations to grip force and receptive fields stimulated by preparatory grip forces increase, the neurons of the percentral motor cortex showed very little anticipatory activity compared with either the premotor areas or the cerebellum.

2004 ◽  
Vol 91 (3) ◽  
pp. 1230-1239 ◽  
Author(s):  
Joël Monzée ◽  
Allan M. Smith

Two monkeys were trained to lift and hold an instrumented object at a fixed height for 2.5 s using a precision grip. The device was equipped with load cells to measure both the grip and lifting or load forces. On selected blocks of 20-30 trials, a downward force-pulse perturbation was applied to the object after 1.5 s of stationary holding. The animals were required to resist the perturbation to obtain a fruit juice reward. The perturbations invariably elicited a reflex-like, time-locked increase in grip force at latencies between 50 and 100 ms. In this study, we searched for single cells in the interpositus and dentate nuclei with activity related to grasping and lifting, and we tested 127/150 task-related cells for their responses to the perturbation. Of the 127 cells, reflex-like increases or decreases in discharge frequency occurred in 75 cells (59%) at a mean latency of 36 ms. Preparatory increases in grip force preceding the perturbation appeared gradually and increased in strength with repetition in 39/127 (31%) cells. These preparatory increases did not immediately disappear when the perturbations were withdrawn but decreased progressively over repeated trials. Although a few cells showed anticipatory activity without a reflex-like response (15/127 or 12%), the majority of these cells (24/39) displayed both anticipatory and reflex-like responses. From an examination of the histological sections, cells with both anticipatory and reflex-like responses appeared to be confined to the dorsal anterior interpositus, adjacent to, but not within, the dentate nucleus. These results confirm and extend the suggestion by Dugas and Smith that the cerebellum plays a major role in organizing anticipatory responses to predictable perturbations in a manner that medial and lateral premotor areas of the cerebral cortex do not.


1995 ◽  
Vol 73 (6) ◽  
pp. 2563-2567 ◽  
Author(s):  
S. H. Scott ◽  
J. F. Kalaska

1. Neuronal activity was recorded in the motor cortex of a monkey that performed reaching movements with the use of two different arm postures. In the first posture (control), the monkey used its natural arm orientation, approximately in the sagittal plane. In the second posture (abducted), the monkey had to adduct its elbow nearly to shoulder level to grasp the handle. The path of the hand between targets was similar in both arm postures, but the joint kinematics and kinetics were different. 2. In both postures, the activity of single cells was often broadly tuned with movement direction and static arm posture over the targets. In a large proportion of cells, either the level of tonic activity, the directional tuning, or both, varied between the two postures during the movement and target hold periods. 3. For most directions of movement, there was a statistically significant difference in the direction of the population vector for the two arm postures. Furthermore, whereas the population vector tended to point in the direction of movement for the control posture, there was a poorer correspondence between the direction of movement and the population vector for the abducted posture. These observed changes are inconsistent with the notion that the motor cortex encodes purely hand trajectory in space.


2001 ◽  
Vol 86 (3) ◽  
pp. 1079-1085 ◽  
Author(s):  
Marie-Josée Boudreau ◽  
Allan M. Smith

The purpose of this investigation was to characterize the discharge of neurons in the rostral area 4 motor cortex (MI) during performance of a precision grip task. Three monkeys were trained to grasp an object between the thumb and index finger and to lift and hold it stationary for 2–2.5 s within a narrow position window. The grip and load forces and the vertical displacement of the object were recorded on each trial. On some trials a downward force-pulse perturbation generating a shear force and slip on the skin was applied to the object after 1.5 s of static holding. In total, 72 neurons were recorded near the rostral limit of the hand area of the motor cortex, located close to the premotor areas. Of these, 30 neurons were examined for receptive fields, and all 30 were found to receive proprioceptive inputs from finger muscles. Intracortical microstimulation applied to 38 recording sites evoked brief hand movements, most frequently involving the thumb and index finger with an average threshold of 12 μA. Slightly more than one-half of the neurons (38/72) demonstrated significant increases in firing rate that on average began 284 ± 186 ms before grip onset. Of 54 neurons tested with predictable force-pulse perturbations, 29 (53.7%) responded with a reflexlike reaction at a mean latency of 54.2 ± 16.8 ms. This latency was 16 ms longer than the mean latency of reflexlike activity evoked in neurons with proprioceptive receptive fields in the more caudal motor cortex. No neurons exhibited anticipatory activity that preceded the perturbation even when the perturbations were delivered randomly and signaled by a warning stimulus. The results indicate the presence of a strong proprioceptive input to the rostral motor cortex, but raise the possibility that the afferent pathway or intracortical processing may be different because of the slightly longer latency.


2002 ◽  
Vol 88 (4) ◽  
pp. 1791-1814 ◽  
Author(s):  
Sylvain Lavoie ◽  
Trevor Drew

We have examined the contribution of the red nucleus to the control of locomotion in the cat. Neuronal activity was recorded from 157 rubral neurons, including identified rubrospinal neurons, in three cats trained to walk on a treadmill and to step over obstacles attached to the moving belt. Of 72 neurons with a receptive field confined to the contralateral forelimb, 66 were phasically active during unobstructed locomotion. The maximal activity of the majority of neurons (59/66) was centered around the swing phase of locomotion. Slightly more than half of the neurons (36/66) were phasically activity during both swing and stance. In addition, some rubral neurons (14/66) showed multiple periods of phasic activity within the swing phase of the locomotor cycle. Periods of phasic discharge temporally coincident with the swing phase of the ipsilateral limb were observed in 7/66 neurons. During voluntary gait modifications, most forelimb-related neurons (70/72) showed a significant increase in their discharge activity when the contralateral limb was the first to step over the obstacle (lead condition). Maximal activity in nearly all cells (63/70) was observed during the swing phase, and 23/63 rubral neurons exhibited multiple increases of activity during the modified swing phase. A number of cells (18/70) showed multiple periods of increased activity during swing and stance. Many of the neurons (35/63, 56%) showed an increase in activity at the end of the swing phase; this period of activity was temporally coincident with the period of activity in wrist dorsiflexors, such as the extensor digitorum communis. A smaller proportion of neurons with receptive fields restricted to the hindlimbs showed similar characteristics to those observed in the population of forelimb-related neurons. The overall characteristics of these rubral neurons are similar to those that we obtained previously from pyramidal tract neurons recorded from the motor cortex during an identical task. However, in contrast to the results obtained in the rubral neurons, most motor cortical neurons showed only one period of increased activity during the step cycle. We suggest that both structures contribute to the modifications of the pattern of EMG activity that are required to produce the change in limb trajectory needed to step over an obstacle. However, the results suggest an additional role for the red nucleus in regulating intra- and interlimb coordination.


1991 ◽  
Vol 66 (2) ◽  
pp. 429-443 ◽  
Author(s):  
P. Burbaud ◽  
C. Doegle ◽  
C. Gross ◽  
B. Bioulac

1. The properties of parietal neurons were studied in four adult rhesus monkeys during fast arm movements. The animals were trained to perform flexion or extension of the forearm about the elbow in response to specific auditory cues. Single neuron activity was recorded in 272 area 5 neurons, 81 neurons of the somatosensory cortex, and 92 neurons of the motor cortex. 2. In area 5, 42% of neuronal changes occurred before movement onset (early changes) and 58% after (late changes), with 21% before the earliest electromyogram. The range of modification in activity took place between 260 ms before movement onset and 180 ms after. Complex receptive fields were found in area 5 with a greater proportion among the late neurons (72%) than among the early neurons (32%). 3. Different patterns of activity were observed in neurons recorded in both movement directions. Reciprocal neurons represented 52% of the motor cortex neurons and 41% of the neurons in the somatosensory cortex but only 14% of the area 5 neurons. Of the remainder area 5 neurons, 46% were direction-sensitive neurons and 39% coactivated neurons. This suggests a more complex encoding of movement direction in area 5 than in area 2 or 4. 4. Temporal characteristics of the neuronal bursts were quantitatively analyzed in areas 5, 2, and 4. Neuronal burst duration was longer in area 5 than in the other areas. Above all, a variability of burst parameters, which did not depend on variable movement execution, was noticed in area 5. Therefore neuronal activity in this cortical area cannot be simply explained by a convergence of sensory and motor inputs but may depend on the behavioral context in which the movement is performed. 5. A correlation between neuronal burst duration and movement duration was found in 41% of area 2 neurons. In area 5, this correlation was observed in 20% of the late neurons and in 14% of the early neurons. A correlation between neuronal discharge frequency and movement velocity was found in 34% of area 2 neurons and 24% of area 4 neurons. About 16% of both late and early neurons in area 5 showed such a correlation. These neurons received polyarticular input, and it is suggested that they may be involved in the kinematic encoding of polyarticular movements. 6. A topographic and functional organization of area 5 was noticed. In anterior area, 5, 83% of the neurons had receptive fields and most of the reciprocal neurons and those exhibiting a correlation with movement parameters were found there.(ABSTRACT TRUNCATED AT 400 WORDS)


1982 ◽  
Vol 48 (4) ◽  
pp. 1048-1057 ◽  
Author(s):  
H. Asanuma ◽  
R. S. Waters ◽  
H. Yumiya

1. The corticocortical projection from area 3a to area 4 gamma was restudied using tranquilized cats. 2. Intracortical microstimulation (ICMS) of a given locus in area 3a produced effects on neurons in area 4 gamma that were located in a small area extending along the direction of the radial fibers constituting a columnar shape. 3. Cortical neurons in area 3a that projected to a particular neuron in area 4 gamma were located in a region that extended along the direction of the radial fibers and constituted a columnar shape. 4. Two-thirds of the projection neurons in area 3a had different receptive fields from those of neurons in the projected area in 4 gamma, thus suggesting that the 3a neurons are not simply transferring peripheral information to the 4 gamma neurons. 5. ICMS delivered to area 3a rarely excited 4 gamma neurons but rather facilitated their evoked discharges. 6. It is suggested that the activity of corticocortical projection from area 3a to 4 gamma can influence the activity of 4 gamma neurons only when combined with other inputs to the motor cortex.


2012 ◽  
Vol 107 (7) ◽  
pp. 1890-1903 ◽  
Author(s):  
Erik E. Stout ◽  
Irina N. Beloozerova

During locomotion, motor cortical neurons projecting to the pyramidal tract (PTNs) discharge in close relation to strides. How their discharges vary based on the part of the body they influence is not well understood. We addressed this question with regard to joints of the forelimb in the cat. During simple and ladder locomotion, we compared the activity of four groups of PTNs with somatosensory receptive fields involving different forelimb joints: 1) 45 PTNs receptive to movements of shoulder, 2) 30 PTNs receptive to movements of elbow, 3) 40 PTNs receptive to movements of wrist, and 4) 30 nonresponsive PTNs. In the motor cortex, a relationship exists between the location of the source of afferent input and the target for motor output. On the basis of this relationship, we inferred the forelimb joint that a PTN influences from its somatosensory receptive field. We found that different PTNs tended to discharge differently during locomotion. During simple locomotion shoulder-related PTNs were most active during late stance/early swing, and upon transition from simple to ladder locomotion they often increased activity and stride-related modulation while reducing discharge duration. Elbow-related PTNs were most active during late swing/early stance and typically did not change activity, modulation, or discharge duration on the ladder. Wrist-related PTNs were most active during swing and upon transition to the ladder often decreased activity and increased modulation while reducing discharge duration. These data suggest that during locomotion the motor cortex uses distinct mechanisms to control the shoulder, elbow, and wrist.


1992 ◽  
Vol 68 (5) ◽  
pp. 1867-1881 ◽  
Author(s):  
N. Picard ◽  
A. M. Smith

1. Two monkeys were trained to grasp an object between the thumb and index finger and lift it to a vertical distance of 12-25 mm. Up to 12 different conditions defined by different combinations of object weights (15, 65, and 115 g) and four surface textures (oiled metal, smooth metal, fine and coarse sandpaper) were used. The apparatus was equipped to measure grip (prehensile) force, vertical (load) force, and object displacement. 2. The monkeys appropriately scaled the grip force for the weight and the coefficient of friction of the object. However, during the dynamic phase of the task (grasping and lifting), the monkeys increased the prehensile force in multiple steps, suggesting that they relied on sensory feedback from the fingers to attain an adequate grip force to lift the object rather than programming the lift in advance. 3. Single-unit activity of 248 neurons was recorded in the hand area of the primary motor cortex while the monkeys performed the task. Of 208 neurons tested for cutaneous and proprioceptive receptive fields (RFs), 96 were sensitive to cutaneous stimulation of the glabrous skin of the hand, whereas 82 received proprioceptive input from wrist and finger muscles. The concentration of neurons with cutaneous input was significantly greater in the rostral bank of the central sulcus compared with cells with proprioceptive RFs, which were more concentrated in the convexity of the precentral gyrus. 4. From the global sample, 199 cells were tested with the three object weights, and 128 of these with at least two surface textures were used in combination with the object weights. The discharge of 58/199 (29%) cells was modulated with the object weight. Cells with cutaneous (20/84, 24%) and proprioceptive (23/71, 32%) RFs were about equally responsive to the object weight. 5. A greater number of motor cortical neurons were influenced by surface texture than by object weight. Of 128 cells tested with at least two surface textures, 67 (52%) showed a modulation of their activity as a function of texture. A significantly greater proportion of neurons with cutaneous RFs (40/63, 63%) showed differential activity as a function of object texture than cells receiving proprioceptive input (21/47, 45%). 6. Weight- and texture-related neurons were not distributed equally in the rostrocaudal dimension of the motor cortex. Only 8% of texture-related cells were located in the convexity of the precentral gyrus, whereas 30% of weight-related neurons were recorded from this rostral zone.(ABSTRACT TRUNCATED AT 400 WORDS)


2019 ◽  
Author(s):  
Eric M. Trautmann ◽  
Daniel J. O’Shea ◽  
Xulu Sun ◽  
James H. Marshel ◽  
Ailey Crow ◽  
...  

AbstractCalcium imaging has rapidly developed into a powerful tool for recording from large populations of neurons in vivo. Imaging in rhesus macaque motor cortex can enable the discovery of new principles of motor cortical function and can inform the design of next generation brain-computer interfaces (BCIs). Surface two-photon (2P) imaging, however, cannot presently access somatic calcium signals of neurons from all layers of macaque motor cortex due to photon scattering. Here, we demonstrate an implant and imaging system capable of chronic, motion-stabilized two-photon (2P) imaging of calcium signals from in macaques engaged in a motor task. By imaging apical dendrites, some of which originated from deep layer 5 neurons, as as well as superficial cell bodies, we achieved optical access to large populations of deep and superficial cortical neurons across dorsal premotor (PMd) and gyral primary motor (M1) cortices. Dendritic signals from individual neurons displayed tuning for different directions of arm movement, which was stable across many weeks. Combining several technical advances, we developed an optical BCI (oBCI) driven by these dendritic signals and successfully decoded movement direction online. By fusing 2P functional imaging with CLARITY volumetric imaging, we verify that an imaged dendrite, which contributed to oBCI decoding, originated from a putative Betz cell in motor cortical layer 5. This approach establishes new opportunities for studying motor control and designing BCIs.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Eric M. Trautmann ◽  
Daniel J. O’Shea ◽  
Xulu Sun ◽  
James H. Marshel ◽  
Ailey Crow ◽  
...  

AbstractCalcium imaging is a powerful tool for recording from large populations of neurons in vivo. Imaging in rhesus macaque motor cortex can enable the discovery of fundamental principles of motor cortical function and can inform the design of next generation brain-computer interfaces (BCIs). Surface two-photon imaging, however, cannot presently access somatic calcium signals of neurons from all layers of macaque motor cortex due to photon scattering. Here, we demonstrate an implant and imaging system capable of chronic, motion-stabilized two-photon imaging of neuronal calcium signals from macaques engaged in a motor task. By imaging apical dendrites, we achieved optical access to large populations of deep and superficial cortical neurons across dorsal premotor (PMd) and gyral primary motor (M1) cortices. Dendritic signals from individual neurons displayed tuning for different directions of arm movement. Combining several technical advances, we developed an optical BCI (oBCI) driven by these dendritic signalswhich successfully decoded movement direction online. By fusing two-photon functional imaging with CLARITY volumetric imaging, we verified that many imaged dendrites which contributed to oBCI decoding originated from layer 5 output neurons, including a putative Betz cell. This approach establishes new opportunities for studying motor control and designing BCIs via two photon imaging.


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