What features of limb movements are encoded in the discharge of cerebellar neurons?

Abstract

This review examines the signals encoded in the discharge of cerebellar neurons during voluntary arm and hand movements, assessing the state of our knowledge and the implications for hypotheses of cerebellar function. The evidence for the representation of forces, joint torques, or muscle activity in the discharge of cerebellar neurons is limited, questioning the validity of theories that the cerebellum directly encodes the motor command. In contrast, kinematic parameters such as position, direction, and velocity are widely and robustly encoded in the activity of cerebellar neurons. These findings favor hypotheses that the cerebellum plans or controls movements in a kinematic framework, such as the proposal that the cerebellum provides a forward internal model. Error signals are needed for on-line correction and motor learning, and several hypotheses postulate the need for their representations in the cerebellum. Error signals have been described mostly in the complex spike discharge of Purkinje cells, but no consensus has emerged on the exact information signaled by complex spikes during limb movements. Newer studies suggest that simple spike firing may also encode error signals. Finally, Purkinje cells located more posterior and laterally in the cerebellar cortex and dentate neurons encode nonmotor, task-related signals such as visual cues. These results suggest that cerebellar neurons provide a complement of information about motor behaviors. We assert that additional single unit studies are needed using rich movement paradigms, given the power of this approach to directly test specific hypotheses about cerebellar function.

Fig. 1

PC simple spike activity during circular tracking. Using a two-joint manipulandum to control a cursor (“+”, 0.5×0.5 cm), monkeys tracked a target (2.5 cm diameter) moving in a circular trajectory (5 cm radius) for 360° in the counterclockwise (CCW; left panel) or clockwise (CW; right panel) directions. The 12×12-cm position workspace (−6 to 6 cm) was partitioned into X–Y bins at a resolution of 0.5×0.5 cm. Simple spike activity was averaged relative to hand position within each bin. Color coding depicts the average change in simple spike firing rate relative to the mean firing rate at each position bin. Arrows point to the position of the maximal simple spike activity (245° for CCW and 25° for CW). Paradigm and experimental details have been described in previous publications [32, 38]

Fig. 2

Simple spike activity is phase locked to hand movements during circular tracking with a visuomotor offset. a For each trial, a constant offset (θ) randomly selected from five values was introduced between the angular position of the manipulandum and the hand representation on the screen. b, c The simple spike activity was binned in 5° bins relative to the hand (b) or target (c) angular position, and then averaged across similar trials (same tracking direction and offset value). Firing modulation and phase is unaffected by the offsets when binned relative to hand position (b). However, the phase for each offset value is markedly shifted when binned relative to target position (c). d The magnitude of the offset effect was quantified as the phase shift between −45° and 45° offsets for each tracking direction. The population summary (n=16; mean±SEM) shows the average offset effect is small when neural activity is binned relative to hand (white bars, 7.8± 15.9°CCW and 2.2±10.1°CW) versus target position (gray bars, 59.7± 14.4°CCW and 50.3±13.7°CW) for both directions of tracking (p=0.028 CCW; p=0.023 CW, paired t test)