Position, Direction of Movement, and Speed Tuning of Cerebellar Purkinje Cells during Circular Manual Tracking in Monkey

Abstract

The cerebellum plays an essential role in pursuit tracking with the eye and with the hand. During smooth pursuit eye movements, both tracking position and velocity are signaled by Purkinje cells. Purkinje cell simple spike discharge is also modulated by direction and speed during linear manual tracking. This study evaluated how all three parameters, position, movement direction, and speed, are signaled in the simple spike discharge of Purkinje cells during circular manual tracking. Three rhesus monkeys intercepted and then tracked a target moving in a circle in both counterclockwise and clockwise directions across a range of constant target speeds. Two sets of analyses of the simple spike firing of 97 Purkinje cells examined the effects of position, movement direction, and speed. The first approach was the incremental improvement of regression models, initially modeling a pure position dependence, then incorporating movement direction, and finally incorporating speed dependence. The second was a modelindependent approach, without any explicit assumptions about the character of the directional tuning or speed effects. Both analyses revealed the same three results: (1) Purkinje cell discharge is spatially tuned, to both the position and direction of movement, and (2) this spatial tuning is not altered by the speed, except (3) the speed scales the average firing and/or depth of modulation.The results suggest that the population of Purkinje cells forms a representation of the entire position-direction space of arm movements, and that the speed modulates the scale of that representation. This speed scaling provides insights into the cerebellar processing of movement-related timing.

Dynamic updating of distributed neural representations using forward models

“…For instance, by using such a mechanism, the overall integration time of gain fields would be reduced drastically and thus would result in more efficient sensorimotor transformations. Moreover, neurons having a preferential tuning to position and velocity like those of our model have been found in the cerebellum (Roitman et al 2005), a brain area suggested to be involved in both the inverse and forward control of movements (Miall and Reckess 2002;Vercher and Gauthier 1988;Wolpert and Kawato 1998). Therefore, in addition to the suggested role of neurons of the cerebellum and of motor cortices in the direct control of movements (Georgopoulos 1996;Schweigenhofer et al 1998;Todorov 2000), their sensitivity to nonlinear mixtures of information, such as arm position and velocity, may also suggest an intrinsic dynamic process within a cortical column.…”

“…Neurophysiological findings also indicate that large groups of neurons in the cerebellum display a preferential tuning to arm position and movement direction. These neurons also fire with almost no latency when compared to real arm dynamics (Fu et al 1997;Roitman et al 2005). Together, these results highly suggest that the brain may use internal forward models in order to predict the consequences of upcoming movements.…”

“…It has also been observed that this group of neurons displays a fast updating of its representation according to motor efference copies or vestibular inputs (Sharp et al 2001). Moreover, in other brain regions, neural representations encoding for different sensory states have also been shown to exhibit a similar updating (Roitman et al 2005;Schwartz and Moran 1999).…”

“…For instance, in an eye-tracking of a self-moved target experiment, it has been shown that, when the subjects actively move a target, the presence of the movement sensory feedback is not necessary to achieve almost zero latency, in contrast to the motor efference copies (Vercher et al 1991). Furthermore, when considering neurophysiological data, predictive neural responses were found in the monkey visual, parietal, and frontal cortices and in the cerebellum (Nakamura and Colby 2002;Roitman et al 2005;Unema and Goldberg 1997), highly suggesting the presence of forward control.…”

“…For instance, the position and the velocity of either a visual stimulus in retinal space or the hand location in cartesian or joint space may be considered. Indeed, real populations of neurons with such a tuning property have been found in several brain areas, such as the motor, parietal, visual, and temporal cortices and in the cerebellum (Ben Hamed et al 2003;Hubel and Wiesel 1977;Jellema et al 2004;Kettner et al 1988;Roitman et al 2005). The modeling novelties that we introduce in this paper are threefold.…”