Encoding of movement time by populations of cerebellar Purkinje cells

Abstract

One of the earliest computational principles attributed to the cerebellum was the measurement of time. This idea was originally suggested on anatomical grounds, and was taken up again to explain some of the deficits in cerebellar patients. The contribution of the cerebellum to eye movements, in contrast, has traditionally been discussed in the context of motor learning. This view has received support from the loss of saccade adaptation, one of the key examples of motor learning, following lesions of the posterior cerebellar vermis. However, the relationship between the properties of saccade-related vermal Purkinje cells and the behavioural deficits that follow lesions is unclear. Here we report results from single-unit recording experiments on monkeys that reconcile the seemingly unrelated concepts of timing and motor learning. We report that, unlike individual Purkinje cells, the population response of larger groups of Purkinje cells gives a precise temporal signature of saccade onset and offset. Thus a vermal population response may help to determine saccade duration. Modifying the time course of the population response by changing the weights of the contributing individual Purkinje cells, discharging at different times relative to the saccade, would directly translate into changes in saccade amplitude.

Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

“…In both figures, the PB is plotted as it develops over time (x axis) for saccades of 45-75 ms durations (y axis). In full accordance with our previous report (9), the two figures show that-independently of the composition of the PC groups-the PB starts 50 ms before saccade onset, peaks at saccade onset, and ends at the time the saccade ends, independently of the duration of the saccade. The tight temporal relationship between burst end and saccade end is expressed by the almost perfect linear regression between the two variables (Fig.…”

“…Actually, we were recently able to provide support for the idea that information from PCs is read out in a population format in a study of normal visually guided saccades. In this study, unlike the saccade-related bursts of individual PCs, the calculated collective instantaneous discharge rate (population burst) of larger group of PCs gave a precise description of the timing of saccades (9). With these considerations in mind, we computed population responses for the two groups of PCs studied during inward and outward adaptation, respectively, and scrutinized their behavior during saccadic adaptation (Fig.…”

“…Burst onset and offset were defined by a 4 ϫ baseline criterion (9). The preadaptation PB is shown in Fig.…”

“…This remapping depends on the integrity of the oculomotor vermis (OV), comprising lobuli VI and VII, as indicated by the fact that experimental lesions cause an irreversible loss of STSA (5,6) and related forms of saccadic learning (7). The OV is characterized by a high density of saccaderelated Purkinje cells (PCs) (8)(9)(10) and low thresholds for microstimulation-evoked saccades (11)(12)(13)(14). Many PCs in the OV fire saccade-related simple spike (SS) bursts that collectively encode the duration of normal, unadapted saccadic eye movements (9).…”

“…The OV is characterized by a high density of saccaderelated Purkinje cells (PCs) (8)(9)(10) and low thresholds for microstimulation-evoked saccades (11)(12)(13)(14). Many PCs in the OV fire saccade-related simple spike (SS) bursts that collectively encode the duration of normal, unadapted saccadic eye movements (9). Two arguments suggest that the tight correlation between the vermal SS population activity and saccade duration may actually reflect a causal role of the population signal in changing saccade metrics as a consequence of STSA by stopping the saccade at the right point in time.…”