Complex Spike Activity of Purkinje Cells in the Oculomotor Vermis during Behavioral Adaptation of Monkey Saccades

Abstract

Throughout life, the oculomotor system can correct itself when saccadic eye movements become inaccurate. This adaptation mechanism can be engaged in the laboratory by displacing the target when the saccade toward it is in flight. Forward and backward target displacements cause gradual increases and decreases in saccade amplitude, respectively. Equipped with this paradigm, we asked whether Purkinje cells (P-cells) in the vermis of the oculomotor cerebellum, lobules VIc and VII, changed their complex spike (CS) discharge during the behavioral adaptation of horizontal saccades. We tested the hypothesis that CS activity would change only when a targeting saccade caused an error in eye position relative to the target, i.e., during the error interval between the primary and corrective saccades. We examined only those P-cells whose simple spike activity exhibited either a burst or pause with saccades in several directions. Approximately 80% of such P-cells exhibited an increase in CS activity during the error interval when the adaptation paradigm imposed horizontal eye-position errors in one direction and a decrease in activity for errors in the other. As adaptation progressed and errors were reduced, there was no consistent change in the CS activity. These data suggest that the CS activity of P-cells in the oculomotor vermis signals the direction but not the magnitude of eye-position error during saccade adaptation. Our results are consistent with cerebellar learning models that have been proposed to explain adaptation of the vestibulo-ocular reflex so similar mechanisms may also underlie plasticity of this precision voluntary oculomotor behavior.

Complex Spike Activity in the Oculomotor Vermis of the Cerebellum: A Vectorial Error Signal for Saccade Motor Learning?

“…In our previous study (Soetedjo and Fuchs 2006), we reported that the CS activity in the interval between the end of dysmetric primary saccades and the onset of the subsequent corrective saccades either increased or decreased during saccade adaptation. Because of the limitations of the behavioral paradigm used in that experiment, we could only determine whether the CS activity preferred left-or rightward error directions, and we also were unable to control error size systematically.…”

“…We surgically implanted a scleral search coil on one eye to measure eye position with an electromagnetic technique (Fuchs and Robinson 1966;Robinson 1963) and stabilization lugs on the skull to prevent head movements. Once the monkeys had recovered from the surgery, they were placed in a dimly lit room and trained to make saccades to a jumping target spot that moved every 1-1.5 s and to fixate the target for from 0.4 to 1s, not including their reaction times, in return for an applesauce reward (Soetedjo and Fuchs 2006). The target was either the image of a red laser spot reflected from two mirror galvanometers (target diameter ϭ 0.4°) onto a cylindrical drum surrounding the monkey or one of many light emitting diodes that were attached to a sphere facing the monkey.…”

“…We sampled horizontal and vertical eye and target position at 1 kHz and unit activity at 50 kHz using a Power 1401 digitizer (Cambridge Electronic Design, Cambridge, UK). The raw digitized data were scrolled by on a computer monitor while, at the same time, the digitizer software, running in Spike2, performed several on-line analyses (Soetedjo and Fuchs 2006). It detected the occurrence of saccades by a velocity criterion (75°/s) and determined saccade amplitude and direction.…”

“…After the saccade was detected, saccade onset and offset were marked for analysis when eye velocity first exceeded and later fell below 20°/s. It also identified the occurrence of a SS when the action potential exceeded a threshold set by the investigators and displayed SS histograms associated with 15°saccades in all eight directions on-line (Soetedjo and Fuchs 2006;their Fig. 3).…”

Head-Unrestrained Gaze Adaptation in the Rhesus Macaque

“…The deeper layers of the SC are connected to the medioposterior cerebellum (caudal fastigial nucleus and oculomotor vermis; Ohtsuka and Noda 1990) via nucleus reticularis tegmenti pontis (NRTP; May et al 1990;Ohtsuka and Noda 1990) and dorsal lateral pontine nucleus (Thier and Mock 2005). Lesions to the medioposterior cerebellum impair rapid saccade amplitude adaptation during the McLaughlin task (Barash et al 1999;Robinson et al 2002;Takagi et al 2000) and the burst metrics of neurons in NRTP (Takeichi et al 2005), caudal fastigial nucleus (Inaba et al 2003;Scudder and McGee 2003), and oculomotor vermis (Catz et al 2005(Catz et al , 2008Soetedjo and Fuchs 2006) are altered along with saccade amplitude during head-restrained saccadic adaptation. Future studies are required to classify the types of motor command signals (gaze, eye, or head) represented at each level of this circuit prior to describing modifications to these signals during gaze adaptation using the McLaughlin task.…”