The same oculomotor vermal Purkinje cells encode the different kinematics of saccades and of smooth pursuit eye movements

Abstract

Saccades and smooth pursuit eye movements (SPEM) are two types of goal-directed eye movements whose kinematics differ profoundly, a fact that may have contributed to the notion that the underlying cerebellar substrates are separated. However, it is suggested that some Purkinje cells (PCs) in the oculomotor vermis (OMV) of monkey cerebellum may be involved in both saccades and SPEM, a puzzling finding in view of the different kinematic demands of the two types of eye movements. Such ‘dual’ OMV PCs might be oddities with little if any functional relevance. On the other hand, they might be representatives of a generic mechanism serving as common ground for saccades and SPEM. In our present study, we found that both saccade- and SPEM-related responses of individual PCs could be predicted well by linear combinations of eye acceleration, velocity and position. The relative weights of the contributions that these three kinematic parameters made depended on the type of eye movement. Whereas in the case of saccades eye position was the most important independent variable, it was velocity in the case of SPEM. This dissociation is in accordance with standard models of saccades and SPEM control which emphasize eye position and velocity respectively as the relevant controlled state variables.

Short-term adaptation of saccades does not affect smooth pursuit eye movement initiation

“…In order to test this expectation, we subjected two monkeys to a standard saccadic adaption paradigm with SPEM test trials at the end and, alternatively, the same two monkeys plus a third one to a random saccadic adaptation paradigm with interleaved trials of SPEM. In contrast to our expectation, we observed at best marginal transfer Citation: Sun, Z., Smilgin, A., Junker, M., Dicke, P. W., & Thier, P. (2017). Short-term adaptation of saccades does not affect smooth pursuit eye movement initiation.…”

“…However, reserving distinct pools of synapses for saccades and for SPEM would only help if also the mossy fiber (MF)-PF signals for saccades and SPEM offered to OMV P-cells formed functionally distinct and anatomically segregated pools. The finding of unrelated preferred directions of P-cell simple spikes for saccades and SPEM would be compatible with this assumption (Sun et al, 2017). However, it is questionable if and to what extent the requirement of segregation is really met.…”

“…In view of the very different kinematic requirements of the two, one might expect that the cerebellar circuits for the control of saccade and SPEM kinematics are separate. Yet, contrary to this expectation, recordings from OMV output neurons, i.e., Purkinje cells (P-cells), in monkeys carrying out SPEM or saccades indicate that the OMV encodes the kinematics of both saccades and SPEM (Dash, Catz, Dicke, & Thier, 2012;Sun, Smilgin, Junker, Dicke, & Thier, 2017). As a matter of fact, rather than deploying distinct sets of P-cells, one tuned to the parameter space of saccades, a second one to that of SPEM, practically all OMV P-cells with oculomotor sensitivity are tuned to saccades as well as to SPEM (Sun et al, 2017).…”

“…Yet, contrary to this expectation, recordings from OMV output neurons, i.e., Purkinje cells (P-cells), in monkeys carrying out SPEM or saccades indicate that the OMV encodes the kinematics of both saccades and SPEM (Dash, Catz, Dicke, & Thier, 2012;Sun, Smilgin, Junker, Dicke, & Thier, 2017). As a matter of fact, rather than deploying distinct sets of P-cells, one tuned to the parameter space of saccades, a second one to that of SPEM, practically all OMV P-cells with oculomotor sensitivity are tuned to saccades as well as to SPEM (Sun et al, 2017). The OMV P-cell is the substrate of the short-term learning-based adjustment or adaptation of saccades (Catz, Dicke, & Thier, 2008) and of SPEM (Dash & Thier, 2013).…”

“…The search coil allowed the high-resolution measurement of instantaneous eye position by picking up a small, eye position-dependent voltage induced by an alternating magnetic field around the monkey's head (Fuchs & Robinson, 1966;Robinson, 1963). The surgical procedures used were identical with those in previous studies (Sun et al, 2017) and described in more detail there. Briefly, monkeys were anesthetized using a combination of isoflurane and remifentanil while carefully monitoring all vital parameters [body temperature, carbon dioxide, oxygen, blood pressure, electrocardiography (ECG)].…”