Cerebellar Influences on Saccade Plasticity

Abstract

Inaccurate saccades adapt to become more accurate. In this experiment the role of cerebellar output to the oculomotor system in adapting saccade size was investigated. We measured saccade adaptation after temporary inactivation of saccade-related neurons in the caudal part of the fastigial nucleus which projects to the oculomotor brain stem. We located caudal fastigial nucleus neurons with single unit recording and injected 0.1% muscimol among them. Two monkeys received bilateral injections and two monkeys unilateral injections. Unilateral injections made ipsiversive saccades hypermetric (gains >1.5) and contraversive saccades hypometric (gains approximately 0.6). Bilateral injections made both leftward and rightward saccades hypermetric (gains >1.5). During unilateral inactivation neither ipsiversive nor contraversive saccade size adapted after approximately 1,000 saccades. During bilateral inactivation, adaptation was either small or very slow. Most intact monkeys completely adapt after approximately 1,000 saccades to similar dysmetrias produced by intrasaccadic target displacement. After the monkeys receiving bilateral injections made >1,000 saccades in each horizontal direction, we placed them in the dark so that the muscimol dissipated without the monkeys receiving visual feedback about its saccade gain. After the dark period, 20-degree saccades were adapted to be 12% smaller, and 4-degree saccades to be 7% smaller. We expect this difference in adaptation because during caudal fastigial nucleus inactivation, monkeys made many large overshooting saccades and few small overshooting saccades. We conclude from these results that: (1) caudal fastigial nucleus activity is important in adapting dysmetric saccades; and (2) bilateral caudal fastigial nucleus inactivation impairs the relay of adapted signals to the oculomotor system, but it does not stop all adaptation from occurring.

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

“…After monkeys undergo about 1,000 to 1,500 trials, saccade amplitude is either increased or reduced, respectively, so that most adapted saccades land near the final target. These changes resemble those produced in primates by muscle weakening because they are gradual, are specific to the saccades that are adapted, and persist when an adapted animal is placed in the dark for 20 h (Robinson et al 2002;Scudder et al 1998).…”

“…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).…”

“…The CFN, in turn, projects to the BG where its input helps shape the burst sent to ocular motoneurons to produce saccades of different amplitudes (Scudder and McGee 2000). CFN signals are necessary for saccade adaptation because humans (Straube et al 2001) and monkeys (Robinson et al 2002) with lesions of this region fail to adapt. However, if muscimol inactivation of the monkey CFN is allowed to dissipate, an underlying adaptation is revealed, suggesting that plasticity had occurred upstream but could not be expressed through the disabled CFN (Robinson et al 2002).…”

“…CFN signals are necessary for saccade adaptation because humans (Straube et al 2001) and monkeys (Robinson et al 2002) with lesions of this region fail to adapt. However, if muscimol inactivation of the monkey CFN is allowed to dissipate, an underlying adaptation is revealed, suggesting that plasticity had occurred upstream but could not be expressed through the disabled CFN (Robinson et al 2002). Therefore, the CFN is influenced by an adapted upstream command signal whose source currently is unknown.…”

Adaptive Control of Saccades via Internal Feedback

“…Because of its direct projection to the PG, the cFN can strongly influence saccadic control, as revealed by lesion (Vilis and Hore, 1981;Robinson et al, 1993;Iwamoto and Yoshida, 2002) and inactivation (Robinson et al, 2002;Goffart et al, 2004) studies. In particular, unilateral muscimol injections in the cFN causes saccade trajectories to curve toward the lesioned side (Robinson et al, 1993).…”