The influence of motor preparation on the response of cerebellar neurons to limb displacements

Abstract

This study examined the influence of "motor set" on the response of neurons in the deep cerebellar nuclei to peripheral afferent inputs. Two monkeys were trained to perform arm movements which were triggered by imposed displacements of their forelimb. Imposed displacements were generated by a torque motor which was coupled to a handle held by the monkey. The direction of the triggered movements depended on a prior instruction presented to the animal before the onset of the imposed displacement.Single neuron recordings were made from 105 interpositus and 191 dentate neurons whose activity was related to the performance of the task. Forty-three of the interpositus and 46 of the dentate neurons displayed a change in activity within 70 msec of the onset of the imposed displacement. None of these neurons displayed a neural response following the onset of the instruction.The short latency response of most interpositus neurons was related to the parameters of the afferent input generated by the imposed displacements. For more than 60% of the interpositus neurons this response was strongly influenced by the direction of the imposed displacement. None of these responses were markedly altered by the prior instructions.In contrast, the short latency response of 67% of the dentate neurons, although triggered by the imposed displacement, was markedly altered by the "motor set" of the animal. For most of the dentate neurons whose activity was influenced by the animal's "motor set," the neural response was contingent on two factors: (1) the prior instruction given to the animal and (2) the direction of the imposed displacement.In a second set of dentate neurons (13% of those influenced by motor preparation) the characteristics of the short latency response were determined solely by the nature of the prior instruction. For these neurons the imposed displacement served as a trigger for possible changes in the activity. Thus, dentate neuron activity can behave like a motor command signal which is triggered at short latency by a peripheral event but depends on the intent of the animal.

Neural and Electromyographic Correlates of Wrist Posture Control

“…Both motor and cognitive areas are represented, consistent with reported cerebellar involvement in the ongoing control of motor tasks (e.g., visually guided movement; Mushiake and Strick 1993;Strick 1983) as well as in more cognitive functions (e.g., language, problem solving, sensory discrimination) (Gao et al 1996;Kim et al 1994;see Leiner et al 1991 for a review). Future studies integrating robotic tools, immersive multisensory feedback environments and neural recording techniques may provide a means to disambiguate the cerebellum's contributions to sensory information processing and motor command updating in the control of limb posture and movement.…”

“…Both segmental and long-loop reflex actions likely contributed to stabilization because we observed temporal correlation between wrist flexor FCR EMGs and the rate of change in wrist joint angle during RT stabilization at latencies between 20 and 178 ms. Loop delays on the short end of this range are consistent with the presence of M1 responses arising from monosynaptic reflex pathways (Lee and Tatton 1975). Loop delays on the long end of the range are consistent with long-loop responses mediated by transcortical pathways thought to transit primary sensorimotor cortex (Evarts and Tanji 1976;Thach 1978) and the cerebellum (Strick 1978(Strick , 1983Thach 1978). The presence of long-loop reflex action provides a means by which the brain can implement closedloop feedback control over wrist position (Evarts and Fromm 1981;Evarts and Tanji 1976;Miall et al 1993;Strick 1978).…”

“…transcortical neural processing (Evarts and Tanji 1976;Haaland and Harrington 1989;Strick 1983). We sought to test the hypothesis that during stabilization of the wrist, distinct neural mechanisms contribute to the closed-loop feedback control of wrist position and the evaluation/adjustment of controller parameters (e.g., the desired reference wrist angle) in response to persistent performance errors.…”

“…The M1 component has the shortest latency occurring ϳ25 ms after a perturbation and is caused by the monosynaptic (segmental) reflex response to muscle stretch. It is followed in time by the M2 and M3 responses, which occur at latencies between 40 and 100 ms. Single-unit recordings in primates demonstrate that these "long loop" reflex pathways are mediated by supraspinal pathways including neural populations in both the primary sensorimotor cortex (Evarts and Tanji 1976;Thach 1978) and the cerebellum (Strick 1978(Strick , 1983Thach 1978). These neuromuscular responses are important in the compensation for unexpected perturbations because both the segmental (Sinkjaer and Hayashi 1989) and the transcortical "reflex" responses (Evarts and Fromm 1981;Evarts and Tanji 1976;Miall et al 1993;Strick 1978) have been implicated in the moment-by-moment (closed-loop or "on-line") feedback control of joint position.…”

Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks

“…DCN fi ring has been shown to be modulated up to around 100 Hz on average 39 , with some studies reporting maximal frequencies of 450 (ref. 40) and 700 (ref. 38).…”