Cerebellar signals drive motor adjustments and visual perceptual changes during forward and backward adaptation of reactive saccades

Abstract

Saccadic adaptation ($SA$) is a cerebellar-dependent learning of motor commands ($MC$), which aims at preserving saccade accuracy. Since $SA$ alters visual localization during fixation and even more so across saccades, it could also involve changes of target and/or saccade visuospatial representations, the latter ($CDv$) resulting from a motor-to-visual transformation (forward dynamics model) of the corollary discharge of the $MC$. In the present study, we investigated if, in addition to its established role in adaptive adjustment of $MC$, the cerebellum could contribute to the adaptation-associated perceptual changes. Transfer of backward and forward adaptation to spatial perceptual performance (during ocular fixation and trans-saccadically) was assessed in eight cerebellar patients and eight healthy volunteers. In healthy participants, both types of $SA$ altered $MC$ as well as internal representations of the saccade target and of the saccadic eye displacement. In patients, adaptation-related adjustments of $MC$ and adaptation transfer to localization were strongly reduced relative to healthy participants, unraveling abnormal adaptation-related changes of target and $CDv$. Importantly, the estimated changes of $CDv$ were totally abolished following forward session but mainly preserved in backward session, suggesting that an internal model ensuring trans-saccadic localization could be located in the adaptation-related cerebellar networks or in downstream networks, respectively.

A triple distinction of cerebellar function for oculomotor learning and fatigue compensation

“…Because of its circular learning architecture, its visuospatial maps and its CD projection pathway to frontal cortex (Middleton & Strick, 2000), the cerebellum is an ideal candidate to also recalibrate the visuospatial target map and the forward dynamics model. In Cheviet et al (2022), we found first evidence that changes in visuospatial representations during saccadic motor learning are impaired in cerebellar patients.…”

“…Consistent with previous studies (Moidell & Bedell, 1988; Collins et al, 2007; Hernandez, Levitan, Banks, & Schor, 2008; Schnier et al, 2010; Zimmermann & Lappe, 2010; Gremmler et al, 2014; Masselink & Lappe, 2021), we found a small change of V 1 in learning direction for control subjects (inward -0.7 ± 2.0°, t 7 = -1.00, p = .351; outward 1.2 ± 1.8°, t 7 = 1.86, p = .105; Figure 3A-1). Please note that in the analysis of Cheviet et al (2022) (which comprised more trials including those in which the flash was presented with a small distance to the 20° target position), these changes were subtly significant. Accordingly, the visual gain ω v of control subjects adapted by -0.04 ± 0.10 ( t 7 = -1.00, p = .351; Figure 4B) in the inward condition and 0.06 ± 0.09 ( t 7 = 1.86, p = .105; Figure 4D) in the outward condition.…”

“…Figure 5 shows a simulation for 7000 saccades directed towards a 10° goal. We chose the initial visuomotor gains ω v , ω m and ω cd measured for similarly sized saccades in 35 healthy subjects by Masselink and Lappe (2021) because the larger sample size provides a more faithful picture than the initial gains of the healthy group of Cheviet et al (2022). The simulation shows that a loss in saccade peak velocity (that is only partially compensated with γ λ = 0.457) leads to an immediate decline of the motor command M , hence shortening the saccade vector from 9.8° to 8.4°.…”

“…Figure 8 shows a simulation for 7000 saccades directed towards a 10 • goal. We chose the initial visuomotor gains ω v , ω m and ω cd measured for similarly sized saccades in 35 healthy subjects by Masselink and Lappe (2021) because the larger sample size provides a more faithful picture than the initial gains of the healthy group of Cheviet et al (2022).…”

“…Here we use an expanded version of the visuomotor learning model of Masselink and Lappe (2021) to quantify the recalibration of the visuospatial target map, of the inverse model and of the forward dynamics model of eight patients with a neurodegenerative cerebellar disease. Data were taken from Cheviet et al (2022), including eight healthy control subjects. To achieve a deeper understanding of which control processes are perturbed, we expanded the model of Masselink and Lappe (2021) with (1) how changes in the motor command are transposed to saccade kinematics (i.e.…”