Cerebellar-dependent adaptive control of primate saccadic system

Abstract

1. The ability of the central nervous system to compensate for saccadic dysmetria was demonstrated in rhesus monkeys. The behavior of this adaptive mechanism after cerebellar ablations was examined. 2. Monkeys were trained to fixate small target lights. Eye movements were monitored while the animals were seated, with their heads fixed, in a rotating magnetic field. The horizontal recti muscles of one eye were weakened by tenectomy. Saccades made by this weakened eye were hypometric and followed by postsaccadic drift. 3. When the patch was switched so that the weak eye was viewing, the hypometric saccades made by the weak eye gradually became larger, until after 3 days they were essentially orthometric. This indicated that the central nervous system could compensate for a peripheral weakness. 4. The tenectomy operation reduced the strength of the muscles, creating hypometria, and upset the ratio of viscosity to elasticity in the orbit, creating postsaccadic drift in the weak eye. The innervation required to make a saccade has both phasic and tonic components, the so-called pulse and step. The sacccadic repair mechanism increased both the pulse and the step to compensate for the hypometria and also adjusted the ratio of the pulse to the step to eliminate postsaccadic drift. 5. Total cerebellectomies were performed on two monkeys, each of which had one tenectomized eye. These ablations created an enduring saccadic hypermetria and postsaccadic drift in the unoperated eye of both animals. The total cerebellectomy abolished all adaptive repair of the saccadic system. 6. Partial cerebellectomies were performed on two monkeys, each of which had one tenectomized eye. Lesions of the vermis and paravermis (lobes IV-IX) and the fastigial nuclei created an enduring saccadic hypermetria without postsaccadic drift in the unoperated eye of both animals. These lesions abolished adaptive control of the pulse of innervation. Adaptive changes in the step of innervation still occurred, so that postsaccadic drift was always eliminated in the experienced, viewing eye. Thus the midline cerebellum (vermis, paravermis, and fastigial nuclei) appears to be important for repair of saccadic dysmetria, but not for repair of postsaccadic drift. Additional evidence that postsaccadic retinal slip cannot be compensated for in flocculectomized monkeys suggest that the adaptive control of the step may depend on the flocculus. 7. After cerebellar lesions the monkeys were able to make saccades of all amplitudes and directions. The principal deficit in these animals seemed to be that the pulse and step of innervation were no longer appropriate to the target displacement. We conclude that the cerebellum's principal contribution to saccadic eye movements is the adjustment of the gains of the pulse- and step-generating mechanisms. Hence this study supports the hypothesis that repair of dysmetria is a general function of the cerebellum.

Discharge of Monkey Nucleus Reticularis Tegmenti Pontis Neurons Changes During Saccade Adaptation

“…When the paretic eye is occluded, saccades of the normal eye become accurate within a few days whereas saccades of the paretic eye become hypometric (Kommerell et al 1976). Similar results were observed in a patient with a medial rectus paresis (Abel et al 1978) and in monkeys whose horizontal recti of one eye were weakened surgically (Optican and Robinson 1980;Scudder and McGee 2003;Snow et al 1985). Thus, the saccadic system is capable of continuous adaptive control under a wide variety of conditions that produce inaccurate saccades.…”

“…A less-direct route from the SC reaches the BG by a parallel pathway that includes first the nucleus reticularis tegmenti pontis (NRTP) and then the midline oculomotor region of the cerebellum, which consists of the oculomotor vermis and the caudal fastigial nucleus (CFN) to which the vermis projects. This midline oculomotor cerebellum has long been implicated in controlling saccade accuracy because lesions there cause saccades to become dysmetric (Optican and Robinson 1980;Ritchie 1976;Robinson et al 1993;Vilis and Hore 1981).…”

“…Lesions of the oculomotor cerebellum also impair saccade adaptation driven either by the McLaughlin paradigm (Barash et al 1999;Robinson et al 2002;Takagi et al 1998) or muscle weakness (Optican and Robinson 1980). Furthermore, neurons in the CFN change the timing and firing rates of their saccaderelated bursts in association with behavioral decreases in saccade amplitude (Inaba et al 2003;Scudder and McGee 2003).…”

A Mechanism for Savings in the Cerebellum

“…As is the case in our simulations, savings may be explained by considering two sites of plasticity whose reversal during extinction occurs somewhat sequentially. Because cerebellar-mediated motor learning is inherently bidirectional, as shown not only during eyelid conditioning (Scavio and Thompson, 1979) but also during adaptation of the vestibulo-ocular reflex (VOR) (Miles and Eighmy, 1980) and saccades (Optican and Robinson, 1980), mutually reversing mechanisms of learning and extinction seem fitting and intuitive for the cerebellum. However, this may not be true for learning mediated by other brain systems.…”

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

“…The monkey oculomotor system is capable of correcting the amplitudes of saccades, i.e., rapid shifts in the direction of gaze, when a dysmetria is caused by muscle weakness (Optican and Robinson 1980) or behavioral deceptions that cause saccades to seem to be inaccurate (Straube et al 1997). The midline cerebellum, which is part of a parallel route for oculomotor information from the superior colliculus (SC) to reach the premotor brain stem generator for saccades (Harting 1977;Kralj-Hans et al 2007;Noda et al 1990;Yamada and Noda 1987), has been implicated as a structure where signals are adapted to reduce saccade dysmetria.…”