Learning Signals from the Superior Colliculus for Adaptation of Saccadic Eye Movements in the Monkey

Abstract

Vital to motor learning is information about movement error. Using this information, the brain creates neural learning signals that instruct a plasticity mechanism to produce appropriate behavioral learning. Little is known, however, about brain structures that generate learning signals for voluntary movements. Here we show that signals from the superior colliculus (SC) can drive learning in saccadic eye movements in the monkey. Electrical stimulation of the SC deeper layers, subthreshold for evoking saccades, was applied immediately (ϳ60 ms) after the end of horizontal saccades in one or both directions. The target disappeared during saccades and remained invisible for 1 s to eliminate effects of postsaccadic visual information. Repetitive pairing of saccades with SC stimulation produced a marked, two-dimensional shift in movement endpoint relative to the target location. The elicited endpoint shift took a gradual, approximately exponential course over several hundred saccades as in visually induced saccade adaptation. The shift in movement endpoint remained nearly unchanged after stimulation was discontinued, indicating involvement of neuronal plasticity. When both rightward and leftward saccades were paired with stimulation, their endpoints shifted in similar directions. The endpoint shift was directed contralaterally to the stimulated SC. The direction and size of the endpoint shift depended on the stimulation site in the SC. We propose that the SC, a brainstem structure long known to be crucial for saccade execution, is involved in motor learning and sends signals that dictate the direction of adaptive shift in saccade endpoint.

Sensorimotor adaptation error signals are derived from realistic predictions of movement outcomes

“…This agrees well with previous studies that suggest the motor correction does not drive adaptation (Noto and Robinson 2001;Tseng et al 2007;Wallman and Fuchs 1998). Still, it is surprising that motor corrections can be made in the opposite direction from that of gain changes during adaptation in light of studies suggesting that the superior colliculus may be involved in driving adaptation (Kaku et al 2009;Soetedjo et al 2009), since the superior colliculus issues saccade commands to the oculomotor plant. Nevertheless, our data clearly indicate that the motor correction does not influence adaptation.…”

“…In our paradigm we present a constant visual error, but, surprisingly, saccades eventually stop adapting (see also Kaku et al 2009;Robinson et al 2003). That is, although subject performance does not improve (retinal error remains fixed), adaptation reaches an asymptote after some time.…”

Sensorimotor adaptation of saccadic eye movements

“…The involvement of the SC was recently demonstrated by the same team (Kaku et al, 2009). Using the same micro-stimulationsaccade pairing approach and targeting the intermediate layers of the SC, the authors elicited the same adaptive-like changes of saccade endpoint as in the Kojima et al's study (2007).…”

“…Available data on reactive saccade adaptation (see Section 5) consistently imply low-level areas (brainstem and cerebellum), whereas fewer recent studies of voluntary saccades adaptation further suggest the contribution of the same brainstem site (hatched area) and of specific cerebellar (and possibly parietal) sites (grey boxes). Future studies will be necessary to delineate the whole extent of the network subtending plastic changes of reactive and voluntary saccades (the possible contribution of Nucleus Reticularis Tegmenti Pontis, thalamo-cortical pathways and basal ganglia have been omitted here) and to identify the neural substrates encoding the error signals eliciting adaptation (only the recently proposed contribution of the superior colliculus (Kaku et al, 2009) reactive saccades in a target double step paradigm. Continuous electro-oculographic recording of eye position allowed to shift the visual target during saccade execution either systematically over successive trials (adaptation condition) or randomly (control condition).…”

Adaptation and adaptation transfer characteristics of five different saccade types in the monkey

“…Second, there is significant adaptation transfer from targeting saccades to saccades evoked by low-current electrical stimulation of the SC (Edelman and Goldberg 2002;Melis and van Gisbergen 1996). Finally, stimulation of the SC to act as a surrogate error signal induces saccade adaptation artificially (Kaku et al 2009;Soetedjo et al 2009). …”