Responses of Cerebellar Interpositus Neurons to Predictable Perturbations Applied to an Object Held in a Precision Grip

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 These preparatory increases did not immediately disappear when the perturbations were withdrawn but decreased progressively over repeated trials.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.

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Comparing Cerebellar and Motor Cortical Activity in Reaching and Grasping

Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques ◽

10.1017/s0317167100048538 ◽

1993 ◽

Vol 20 (S3) ◽

pp. S53-S61 ◽

Cited By ~ 10

Author(s):

M. Smith Allan ◽

Dugas Clause ◽

Fortier Pierre ◽

Kalasha John ◽

Picard Nathalie

Keyword(s):

Motor Cortex ◽

Cortical Neurons ◽

Grip Force ◽

Single Cells ◽

Receptive Fields ◽

Movement Direction ◽

Arm Reaching ◽

Anticipatory Activity ◽

Motor Strategies ◽

Premotor Areas

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.

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Activity in Rostral Motor Cortex in Response to Predictable Force-Pulse Perturbations in a Precision Grip Task

Journal of Neurophysiology ◽

10.1152/jn.2001.86.3.1079 ◽

2001 ◽

Vol 86 (3) ◽

pp. 1079-1085 ◽

Cited By ~ 21

Author(s):

Marie-Josée Boudreau ◽

Allan M. Smith

Keyword(s):

Motor Cortex ◽

Index Finger ◽

Precision Grip ◽

Receptive Fields ◽

Vertical Displacement ◽

Warning Stimulus ◽

Force Pulse ◽

Pulse Perturbation ◽

Anticipatory Activity ◽

Proprioceptive Inputs

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.

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Effects of Muscimol Inactivation of the Cerebellar Nuclei on Precision Grip

Journal of Neurophysiology ◽

10.1152/jn.01124.2002 ◽

2004 ◽

Vol 91 (3) ◽

pp. 1240-1249 ◽

Cited By ~ 22

Author(s):

Joël Monzée ◽

Trevor Drew ◽

Allan M. Smith

Keyword(s):

Grip Force ◽

Dentate Nucleus ◽

Precision Grip ◽

Three Dimensional ◽

Cerebellar Nuclei ◽

Motor Deficits ◽

Intention Tremor ◽

Interpositus Nucleus ◽

Reversible Inactivation ◽

Cell Recording

A single monkey was trained to perform a grasp, lift, and hold task in which a stationary hand- held object was sometimes subjected to brief, predictable force-pulse perturbations. The displacement, grip, and lifting forces were measured as well the three-dimensional forces and torques to quantify specific motor deficits after reversible inactivation of the cerebellar nuclei. A prior single-cell recording study in the same monkey provided the stereotaxic coordinates used to guide intranuclear injections of muscimol. In total, 34 penetrations were performed at 28 different loci throughout the cerebellar nuclei. On each penetration, two 1.0-μl injections of 5 μg/μl muscimol, were made 1.0 mm apart either within the nuclei or in the white matter just lateral or posterior to the dentate nucleus. Injections in the region corresponding to the anterior interpositus nucleus produced pronounced dynamic tremor and dysmetric movements of the ipsilateral arm when the animal performed unrestrained reaching and grasping movements. In contrast, no relatively short-latency (15-20 min.) deficits were observed after injection in the dentate nucleus, although some effects were observed after several hours. When tested in a primate chair with the forearm supported and restrained at the wrist and elbow, the monkey performed the lift and hold task without tremor or dysmetria. However, with the restraint removed, the forces and torques applied to the manipulandum were poorly controlled and erratic. The monkey's arm was ataxic and a 5-Hz intention tremor was clearly visible. In addition, the animal was generally unable to compensate for the predictable perturbations and the anticipatory grip force increases were absent. However, overall the results suggest that reversible cerebellar nuclear inactivation with muscimol has little effect on isolated distal movements of the wrist and fingers.

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An Unfolded Map of the Cerebellar Dentate Nucleus and its Projections to the Cerebral Cortex

Journal of Neurophysiology ◽

10.1152/jn.00626.2002 ◽

2003 ◽

Vol 89 (1) ◽

pp. 634-639 ◽

Cited By ~ 388

Author(s):

Richard P. Dum ◽

Peter L. Strick

Keyword(s):

Cerebral Cortex ◽

Dentate Nucleus ◽

Neurotropic Viruses ◽

Transneuronal Transport ◽

Posterior Parietal ◽

Cerebellar Dentate Nucleus ◽

Premotor Areas

We have used retrograde transneuronal transport of neurotropic viruses to examine the organization of the projections from the dentate nucleus of the cerebellum to “motor” and “nonmotor” areas of the cerebral cortex. To perform this analysis we created an unfolded map of the dentate. Plotting the results from current and prior experiments on this unfolded map revealed important features about the topography of function in the dentate. We found that the projections to the primary motor and premotor areas of the cerebral cortex originated from dorsal portions of the dentate. In contrast, projections to prefrontal and posterior parietal areas of cortex originated from ventral portions of the dentate. Thus the dentate contains anatomically separate and functionally distinct motor and nonmotor domains.

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Visual and Tactile Information About Object-Curvature Control Fingertip Forces and Grasp Kinematics in Human Dexterous Manipulation

Journal of Neurophysiology ◽

10.1152/jn.2000.84.6.2984 ◽

2000 ◽

Vol 84 (6) ◽

pp. 2984-2997 ◽

Cited By ~ 64

Author(s):

Per Jenmalm ◽

Seth Dahlstedt ◽

Roland S. Johansson

Keyword(s):

Visual Processing ◽

Visual Cues ◽

Grip Force ◽

Center Of Mass ◽

Precision Grip ◽

Sensory Information ◽

Afferent Input ◽

Dependent Manner ◽

Tactile Sensibility ◽

Grasp Stability

Most objects that we manipulate have curved surfaces. We have analyzed how subjects during a prototypical manipulatory task use visual and tactile sensory information for adapting fingertip actions to changes in object curvature. Subjects grasped an elongated object at one end using a precision grip and lifted it while instructed to keep it level. The principal load of the grasp was tangential torque due to the location of the center of mass of the object in relation to the horizontal grip axis joining the centers of the opposing grasp surfaces. The curvature strongly influenced the grip forces required to prevent rotational slips. Likewise the curvature influenced the rotational yield of the grasp that developed under the tangential torque load due to the viscoelastic properties of the fingertip pulps. Subjects scaled the grip forces parametrically with object curvature for grasp stability. Moreover in a curvature-dependent manner, subjects twisted the grasp around the grip axis by a radial flexion of the wrist to keep the desired object orientation despite the rotational yield. To adapt these fingertip actions to object curvature, subjects could use both vision and tactile sensibility integrated with predictive control. During combined blindfolding and digital anesthesia, however, the motor output failed to predict the consequences of the prevailing curvature. Subjects used vision to identify the curvature for efficient feedforward retrieval of grip force requirements before executing the motor commands. Digital anesthesia caused little impairment of grip force control when subjects had vision available, but the adaptation of the twist became delayed. Visual cues about the form of the grasp surface obtained before contact was used to scale the grip force, whereas the scaling of the twist depended on visual cues related to object movement. Thus subjects apparently relied on different visuomotor mechanisms for adaptation of grip force and grasp kinematics. In contrast, blindfolded subjects used tactile cues about the prevailing curvature obtained after contact with the object for feedforward adaptation of both grip force and twist. We conclude that humans use both vision and tactile sensibility for feedforward parametric adaptation of grip forces and grasp kinematics to object curvature. Normal control of the twist action, however, requires digital afferent input, and different visuomotor mechanisms support the control of the grasp twist and the grip force. This differential use of vision may have a bearing to the two-stream model of human visual processing.

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Wrist Action Affects Precision Grip Force

Journal of Neurophysiology ◽

10.1152/jn.1997.78.1.271 ◽

1997 ◽

Vol 78 (1) ◽

pp. 271-280 ◽

Cited By ~ 53

Author(s):

Mary M. Werremeyer ◽

Kelly J. Cole

Keyword(s):

Grip Force ◽

Precision Grip ◽

Load Force ◽

Myoelectric Activity ◽

Resistive Load ◽

Wrist Flexion ◽

Wrist Extension ◽

Hand Muscles ◽

Force Pulse ◽

Grasp Stability

Werremeyer, Mary M. and Kelly J. Cole. Wrist action affects precision grip force. J. Neurophysiol. 78: 271–280, 1997. When moving objects with a precision grip, fingertip forces normal to the object surface (grip force) change in parallel with forces tangential to the object (load force). We investigated whether voluntary wrist actions can affect grip force independent of load force, because the extrinsic finger muscles cross the wrist. Grip force increased with wrist angular speed during wrist motion in the horizontal plane, and was much larger than the increased tangential load at the fingertips or the reaction forces from linear acceleration of the test object. During wrist flexion the index finger muscles in the hand and forearm increased myoelectric activity; during wrist extension this myoelectric activity increased little, or decreased for some subjects. The grip force maxima coincided with wrist acceleration maxima, and grip force remained elevated when subjects held the wrist in extreme flexion or extension. Likewise, during isometric wrist actions the grip force increased even though the fingertip loads remained constant. A grip force “pulse” developed that increased with wrist force rate, followed by a static grip force while the wrist force was sustained. Subjects could not suppress the grip force pulse when provided visual feedback of their grip force. We conclude that the extrinsic hand muscles can be recruited to assist the intended wrist action, yielding higher grip-load ratios than those employed with the wrist at rest. This added drive to hand muscles overcame any loss in muscle force while the extrinsic finger flexors shortened during wrist flexion motion. During wrist extension motion grip force increases apparently occurred from eccentric contraction of the extrinsic finger flexors. The coactivation of hand closing muscles with other wrist muscles also may result in part from a general motor facilitation, because grip force increased during isometric knee extension. However, these increases were related weakly to the knee force. The observed muscle coactivation, from all sources, may contribute to grasp stability. For example, when transporting grasped objects, upper limb accelerations simultaneously produce inertial torques at the wrist that must be resisted, and inertial loads at the fingertips from the object that must be offset by increased grip force. The muscle coactivation described here would cause similarly timed pulses in the wrist force and grip force. However, grip-load coupling from this mechanism would not contribute much to grasp stability when small wrist forces are required, such as for slow movements or when the object's total resistive load is small.

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Neuronal Activity in Somatosensory Cortex of Monkeys Using a Precision Grip. I. Receptive Fields and Discharge Patterns

Journal of Neurophysiology ◽

10.1152/jn.1999.81.2.825 ◽

1999 ◽

Vol 81 (2) ◽

pp. 825-834 ◽

Cited By ~ 28

Author(s):

Iran Salimi ◽

Thomas Brochier ◽

Allan M. Smith

Keyword(s):

Receptive Field ◽

Somatosensory Cortex ◽

Neuronal Activity ◽

Single Cells ◽

Precision Grip ◽

Receptive Fields ◽

Pressure Change ◽

Discharge Pattern ◽

Cortical Cells ◽

Discharge Patterns

Neuronal activity in somatosensory cortex of monkeys using a precision grip. I. Receptive fields and discharge patterns. Three adolescent Macaca fascicularis monkeys weighing between 3.5 and 4 kg were trained to use a precision grip to grasp a metal tab mounted on a low friction vertical track and to lift and hold it in a 12- to 25-mm position window for 1 s. The surface texture of the metal tab in contact with the fingers and the weight of the object could be varied. The activity of 386 single cells with cutaneous receptive fields contacting the metal tab were recorded in Brodmann’s areas 3b, 1, 2, 5, and 7 of the somatosensory cortex. In this first of a series of papers, we describe three types of discharge pattern, the receptive-field properties, and the anatomic distribution of the neurons. The majority of the receptive fields were cutaneous and covered less than one digit, and a χ2 test did not reveal any significant differences in the Brodmann’s areas representing the thumb and index finger. Two broad categories of discharge pattern cells were identified. The first category, dynamic cells, showed a brief increase in activity beginning near grip onset, which quickly subsided despite continued pressure applied to the receptive field. Some of the dynamic neurons responded to both skin indentation and release. The second category, static cells, had higher activity during the stationary holding phase of the task. These static neurons demonstrated varying degrees of sensitivity to rates of pressure change on the skin. The percentage of dynamic versus static cells was about equal for areas 3b, 2, 5, and 7. Only area 1 had a higher proportion of dynamic cells (76%). A third category was identified that contained cells with significant pregrip activity and included cortical cells with both dynamic or static discharge patterns. Cells in this category showed activity increases before movement in the absence of receptive-field stimulation, suggesting that, in addition to peripheral cutaneous input, these cells also receive strong excitation from movement-related regions of the brain.

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