Reduction of rostral dorsal accessory olive responses during reaching

Abstract

1. Rostral dorsal accessory olive (rDAO) neurons are sensitive to light touch but have little or no discharge during active movement. We hypothesize that sensitivity of the rDAO is reduced during movement. To test this hypothesis, we evaluated sensitivity of rDAO neurons as cats reached out and retrieved a handle. On selected trials, mechanical or electrical perturbations to the forelimb were presented, and responses of rDAO neurons to the disturbances were recorded. 2. All rDAO units were highly sensitive to somatosensory stimuli during periods of stance. The cells responded to stimuli such as touch to hairs or light taps to the platform on which the cat was standing. 3. Discharges of rDAO neurons showed little or no synchronization to any aspect of the reaching task. rDAO neurons failed to fire to mechanical perturbations of the food handle during retrieval or hold phases of the task, even when their receptive fields included the surface of the paw in contact with the handle. 4. Electrical stimulation of the skin produced the greatest evoked response at all rDAO recording sites when the cats were at stance. Stimulation at any time during the reaching task, including periods of holding and licking, produced lower-amplitude evoked responses. The reduction in evoked response could be large and was restricted to the limb performing the task. 5. The data support the hypothesis that the cutaneous sensitivity of the rDAO is reduced during behavior. However, the inhibition does not appear to be tailored to specific times during the task or to neurons with specific receptive field locations on the actively moving limb. The reduction in sensitivity is as likely to be dependent on limb posture as on movement. We conclude that the rDAO discharge provides the cerebellum with information about vibration or contact during stance; it does not provide reliable information about undisturbed or disturbed movement. Climbing fiber input from rDAO might be useful in the preparation to make a movement, but it is probably not useful for correction of movement errors.

Role of the Olivo-Cerebellar System in Timing

“…Because the synchronization task required both perception and motor performance of temporal sequences, the "suppression" of the inferior olive response to the perception component of the task can conceivably be attributed to the concurrent motor activity. This interpretation would be most consistent with electrophysiological studies showing that the responsiveness of the olivary neurons to sensory input is mostly decreased during expected self-produced movement (Gellman et al, 1985;Horn et al, 1996;Apps et al, 1997;Gibson et al, 2002). This may further explain the failure to demonstrate inferior olive activation during timing tasks in previous functional imaging studies that mostly used paradigms requiring motor preparation or motor response (Rao et al, 1997;Schubotz et al, 2000;Ramnani and Passingham, 2001;Dhamala et al, 2003).…”

“…However, the primary role of the inferior olive and the climbing fiber system in timing and motor control is poorly understood and remains a matter of debate. One view is that the role of the olivo-cerebellar system in timing and error correction of ongoing movement is limited given the relatively slow intrinsic firing rate of the olivary neurons and their variable responsiveness to active movement (Thach, 1968;Armstrong, 1974;Keating and Thach, 1995;Horn et al, 1996;Gibson et al, 2004). However, it has also been suggested that timing of fast movement and modulation of cerebellar output during movement is accomplished by rhythmic and synchronized firing of ensembles of olivary neurons and their population code rather than individual neuronal oscillations (Welsh et al, 1995;Welsh, 2002).…”

Gating of cutaneous input to cerebellar climbing fibres during a reaching task in the cat

“…This is the first report on gating of cutaneous input to climbing fibres terminating within different paravermal cortical zones during the performance of a well-rehearsed reaching task, adding to previous studies concerned with modulation of input to the inferior olive (Horn et al 1996; see also Gellman et al 1985) and modulation of input to climbing fibres during locomotion Apps et al 1990Apps et al , 1995b. Although not without exceptions, response size was usually progressively reduced during the course of the reaching movement, being smallest when the animal was grasping the food with the limb relatively extended.…”

Functional Relations of Cerebellar Modules of the Cat

“…Cutaneous electrical stimulation (monophasic, square-wave, bipolar, 0.10 ms duration) was used to elicit olivary activity. Evoked olivary activity has variability in timing, polarity, and number of potentials, so the recordings were rectified, integrated (1 ms time constant), digitized (25 kHz sample rate), and averaged across 20 stimulus presentations to provide a reliable estimate of activity (Horn et al, 1996).…”