Cortico-cerebellar network involved in saccade adaptation.

Saccade adaptation is the learning process that ensures that vision and saccades remain calibrated. The central nervous system network involved in these adaptive processes remains unclear because of difficulties in isolating the learning process from the correlated visual and motor processes. Here we imaged the human brain during a novel saccade adaptation paradigm that allowed us to isolate neural signals involved in learning independent of the changes in the amplitude of corrective saccades usually correlated with adaptation. We show that the changes in activation in the ipsiversive cerebellar vermis that track adaptation are not driven by the changes in corrective saccades and thus provide critical supporting evidence for previous findings. Similarly, we find that activation in the dorsomedial wall of the contraversive precuneus mirrors the pattern found in the cerebellum. Finally, we identify dorsolateral and dorsomedial cortical areas in the frontal and parietal lobes that encode the retinal errors following inaccurate saccades used to drive recalibration. Together, these data identify a distributed network of cerebellar and cortical areas and their specific roles in oculomotor learning. NEW & NOTEWORTHY The central nervous system constantly learns from errors and adapts to keep visual targets and saccades in registration. We imaged the human brain while the gain of saccades adapted to a visual target that was displaced while the eye was in motion, inducing retinal error. Activity in the cerebellum and precuneus tracked learning, whereas parts of the dorsolateral and dorsomedial frontal and parietal cortex encoded the retinal error used to drive learning.

Secondary adaptation of memory-guided saccades.

Adaptation of saccade gains in response to errors keeps vision and action co-registered in the absence of awareness or effort. Timing is key, as the visual error must be available shortly after the saccade is generated or adaptation does not occur. Here, we tested the hypothesis that when feedback is delayed, learning still occurs, but does so through small secondary corrective saccades. Using a memory-guided saccade task, we gave feedback about the accuracy of saccades that was falsely displaced by a consistent amount, but only after long delays. Despite the delayed feedback, over time subjects improved in accuracy toward the false feedback. They did so not by adjusting their primary saccades, but via directed corrective saccades made before feedback was given. We propose that saccade learning may be driven by different types of feedback teaching signals. One teaching signal relies upon a tight temporal relation with the saccade and contributes to obligatory learning independent of awareness. When this signal is ineffective due to delayed error feedback, a second compensatory teaching signal enables flexible adjustments to the spatial goal of saccades and helps maintain sensorimotor accuracy.

Obligatory adaptation of saccade gains.

We tested the hypothesis that saccade gains adapt to minimize error between the visual target and the saccade endpoint of every saccade we make even when the errors on sequential saccades are not directionally consistent. We utilized a state-space model that estimated the degree to which saccade gains were modified by the magnitude and direction of errors made on the previous trial. Importantly, to show that learning did not depend on the accumulation of directionally consistent errors, we fit the model to saccades made to targets that were displaced in a random direction during the saccade, thereby inducing errors with directions that were not sequentially the same. Saccade gains clearly adapted on a trial-by-trial basis despite that the perturbations were random, and the average amount of learning per trial was of similar magnitude as that found in a constant displacement of the target. These results indicate that saccade adaptation is a rapid and obligatory process that does not require conscious awareness.

Persistent neural activity during the maintenance of spatial position in working memory.

The mechanism for the short-term maintenance of information involves persistent neural activity during the retention interval, which forms a bridge between the cued memoranda and its later contingent response. Here, we used event-related functional magnetic resonance imaging to identify cortical areas with activity that persists throughout working memory delays with the goal of testing if such activity represents visuospatial attention or prospective saccade goals. We did so by comparing two spatial working memory tasks. During a memory-guided saccade (MGS) task, a location was maintained during a delay after which a saccade was generated to the remembered location. During a spatial item recognition (SIR) task identical to MGS until after the delay, a button press indicated whether a newly cued location matched the remembered location. Activity in frontal and parietal areas persisted above baseline and was greater in the hemisphere contralateral to the cued visual field. However, delay-period activity did not differ between the tasks. Notably, in the putative frontal eye field (FEF), delay period activity did not differ despite that the precise metrics of the memory-guided saccade were known during the MGS delay and saccades were never made in SIR. Persistent FEF activity may therefore represent a prioritized attentional map of space, rather than the metrics for saccades.