Cortico-cerebellar network involved in saccade adaptation

Abstract

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.

Keywords: cerebellum; motor learning; oculomotor vermis; precuneus; saccade adaptation.

Fig. 1.

Modified backstep paradigm used in the present study and behavioral results. A: examples of typical horizontal eye position traces for trials early in the adaptation phase. Gray lines represent target position. Left (blue): the classic backstep paradigm with a backward target step during the saccade, which induces a backward corrective saccade (data from Srimal et al. 2008). Right (red): in our modified paradigm, the backstepped target was presented for only 160 ms and then was placed 0.5° to the left of fixation. B: amplitude of corrective saccades as a function of the trial number across all participants. Mean amplitude was calculated with a sliding window of 10 trials. Shaded areas correspond to ±1 SD. Blue curve corresponds to values obtained with the classic backstep paradigm (data from Srimal et al. 2008) and red curve to values obtained with our modified backstep paradigm. Note how the amplitudes of corrective saccades track learning only in the classic version. C: saccade gain as a function of trial number for a representative participant. An experimental session was divided into 5 phases of 50 trials each: Preadapt, Adapt (A1, A2, A3), and Deadapt. Thin dashed horizontal lines demark the amplitude of the target. Thick solid horizontal lines correspond to mean saccade gain for each phase. Note how saccade gain decreases in each Adapt phase and then rebounds in the Deadapt phase. D: distribution of saccade gain changes from Preadapt to A3 phases for each participant.

Fig. 2.

Cortical and cerebellar activity during visually guided saccades. t-Statistic maps are projected onto an inflated model of the left and right hemispheres of the human brain (lateral and medial views), where dark gray corresponds to the sulcal folds and light gray to the gyral convexities. For the cerebellum, the results are projected on a flat representation of the cerebellum. Roman numerals denote cerebellar lobules according to the Larsell notation (Schmahmann et al. 2000). Note the larger activations in the right cortex and in the left cerebellum during leftward saccades.

Fig. 3.

Cortical and cerebellar activations related to adaptation of saccades. A: results of the group analysis for the contrast between the Preadapt and A1 (Adapt) phases. During the first phase of Adapt when the saccade gain decreased the most, blood oxygen level-dependent (BOLD) signal increased in the oculomotor vermis (lobule VIIa) and on the medial wall of the parietal cortex, in the right precuneus. There was also a decrease in activity in the right cerebellar hemisphere (lobule VIIb/Crus 2). B: mean gain change between these 2 phases for each participant, which was entered as a covariate in the general linear model (see materials and methods). C: for each cluster in A, we graph the covariation between the change in BOLD signal (β) during saccade adaptation and the degree of saccade gain change during adaptation.

Fig. 4.

Activity in contraversive precuneus (A) and supramarginal gyrus (B) track reductions in gain during saccade adaptation.

Fig. 5.

Cortical and cerebellar activations obtained in the parametric analysis based on the size of saccade error introduced by the target step. Blood oxygen level-dependent (BOLD) variations with amplitude correlated to the size of the error were found bilaterally in the calcarine sulcus, in the parieto-occipital sulcus, and on the superior occipital gyrus. One cluster was found in the intraparietal sulcus of the left hemisphere and 2 others in the frontal cortex of the right hemisphere: 1 in the precentral sulcus and 1 on the medial superior frontal gyrus. Activations were also observed in the right anterior insula and in the right temporo-parietal junction. Two clusters were found in the cerebellum (left lobule V and right lobule VI).