Christopher T. Noto

Visual error is the stimulus for saccade gain adaptation

Saccade accuracy is fundamental to clear vision. The brain maintains saccade accuracy by altering commands for saccades that are consistently inaccurate. For example, saccades that consistently overshoot their targets gradually become smaller. The signal that drives the adaptation of saccade size is not well understood. Previous reports propose that corrective movements and visual errors, both generated after inaccurate saccades, could be responsible for a change in saccade size. Here we show that we can elicit normal reductions in saccade size while eliciting few or no correction saccades. These normal reductions in saccade size indicate that visual errors, not correction saccades, drive the adaptation of saccades.

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 ∼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 ∼1,000 saccades. During bilateral inactivation, adaptation was either small or very slow. Most intact monkeys completely adapt after ∼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.

Non-visual information does not drive saccade gain adaptation in monkeys

Recent experiments have characterized the dependence of saccade gain adaptation on the characteristics of the visual error following inaccurate saccades. We currently know little about the potential role of non-visual information in driving saccade adaptation. The brain could use non-visual signals from the saccade burst generator or extraocular muscle (EOM) proprioceptors to determine if the eye had rotated the appropriate distance to aim at a target. Both saccade-related burst signals and EOM proprioceptive information reach the posterior vermis of the cerebellum, a brain area strongly implicated in saccade adaptation. In the experiment described here we determined if non-visual information has a significant affect on saccade adaptation. We made monkey saccades hypometric with intra-saccade target movements and then tested the recovery of saccade gain toward normal under three conditions: (1) when the target was continuously visible, (2) when the target extinguished for 1000 ms beginning during the saccade, and (3) when the monkey remained in the dark. In the first condition both visual and non-visual indications of hypometria were available. In the second, only non-visual information was available. In the third, the monkey made no visually guided saccades and very few spontaneous saccades in the dark so neither visual nor non-visual information could drive adaptation. We found that, though it was hypometric, saccade size during recovery changed the same small amount when monkeys made saccades to extinguishing targets or remained in the dark. Saccade size changed significantly (approximately 5x) more during recovery when the monkey tracked continuously visible targets. Thus non-visual information has no influence on adaptation and visual post-saccade error is the only known driver of saccade adaptation.

Effect of visual background on saccade adaptation in monkeys

The brain maintains saccade accuracy by modifying saccades that are consistently inaccurate (e.g. hypermetric). To determine whether this adaptation is influenced by the visual background we used several different target and background movements to elicit changes in saccade gain. In almost all cases, the target spot drove gain changes. The background had no effect on, or slightly reduced, adaptation. We conclude that the saccade adaptation mechanism is driven almost entirely by stimuli on or near the fovea and is affected very little by visual stimuli falling more peripherally.