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

The cerebellum implements error-based motor learning via synaptic gain adaptation of an inverse model, i.e. the mapping of a spatial movement goal onto a motor command. Recently, we modeled the motor and perceptual changes during learning of saccadic eye movements, showing that learning is actually a threefold process. Besides motor recalibration of (1) the inverse model, learning also comprises perceptual recalibration of (2) the visuospatial target map and (3) of a forward dynamics model that estimates the saccade size from corollary discharge. Yet, the site of perceptual recalibration remains unclear. Here we dissociate cerebellar contributions to the three stages of learning by modeling the learning data of eight cerebellar patients and eight healthy controls. Results showed that cerebellar pathology restrains short-term recalibration of the inverse model while the forward dynamics model is well informed about the reduced saccade change. Adaptation of the visuospatial target map trended in learning direction only in control subjects, yet without reaching significance. Moreover, some patients showed a tendency for uncompensated oculomotor fatigue caused by insufficient upregulation of saccade duration. According to our model, this could induce long-term perceptual compensation, consistent with the overestimation of target eccentricity found in the patients' baseline data. We conclude that the cerebellum mediates short-term adaptation of the inverse model, especially by control of saccade duration, while the forward dynamics model was not affected by cerebellar pathology.

Adaptive changes to saccade amplitude and target localization do not require pre-saccadic target visibility.

The accuracy of saccadic eye movements is maintained by saccadic adaptation, a learning mechanism that is proposed to rely on visual prediction error, i.e., a mismatch between the pre-saccadically predicted and post-saccadically experienced position of the saccade target. However, recent research indicates that saccadic adaptation might be driven by postdictive motor error, i.e., a retrospective estimation of the pre-saccadic target position based on the post-saccadic image. We investigated whether oculomotor behavior can be adapted based on post-saccadic target information alone. We measured eye movements and localization judgements as participants aimed saccades at an initially invisible target, which was always shown only after the saccade. Each such trial was followed by either a pre- or a post-saccadic localization trial. The target position was fixed for the first 100 trials of the experiment and, during the following 200 trials, successively shifted inward or outward. Saccade amplitude and the pre- and post-saccadic localization judgements adjusted to the changing target position. Our results suggest that post-saccadic information is sufficient to induce error-reducing adaptive changes in saccade amplitude and target localization, possibly reflecting continuous updating of the estimated pre-saccadic target location driven by postdictive motor error.

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

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.

Visuomotor learning from postdictive motor error.

Sensorimotor learning adapts motor output to maintain movement accuracy. For saccadic eye movements, learning also alters space perception, suggesting a dissociation between the performed saccade and its internal representation derived from corollary discharge (CD). This is critical since learning is commonly believed to be driven by CD-based visual prediction error. We estimate the internal saccade representation through pre- and trans-saccadic target localization, showing that it decouples from the actual saccade during learning. We present a model that explains motor and perceptual changes by collective plasticity of spatial target percept, motor command, and a forward dynamics model that transforms CD from motor into visuospatial coordinates. We show that learning does not follow visual prediction error but instead a postdictive update of space after saccade landing. We conclude that trans-saccadic space perception guides motor learning via CD-based postdiction of motor error under the assumption of a stable world.

Translation and articulation in biological motion perception.

Recent models of biological motion processing focus on the articulational aspect of human walking investigated by point-light figures walking in place. However, in real human walking, the change in the position of the limbs relative to each other (referred to as articulation) results in a change of body location in space over time (referred to as translation). In order to examine the role of this translational component on the perception of biological motion we designed three psychophysical experiments of facing (leftward/rightward) and articulation discrimination (forward/backward and leftward/rightward) of a point-light walker viewed from the side, varying translation direction (relative to articulation direction), the amount of local image motion, and trial duration. In a further set of a forward/backward and a leftward/rightward articulation task, we additionally tested the influence of translational speed, including catch trials without articulation. We found a perceptual bias in translation direction in all three discrimination tasks. In the case of facing discrimination the bias was limited to short stimulus presentation. Our results suggest an interaction of articulation analysis with the processing of translational motion leading to best articulation discrimination when translational direction and speed match articulation. Moreover, we conclude that the global motion of the center-of-mass of the dot pattern is more relevant to processing of translation than the local motion of the dots. Our findings highlight that translation is a relevant cue that should be integrated in models of human motion detection.