Adaptation Of Voluntary Saccades Research Articles

Effects of structural and functional cerebellar lesions on sensorimotor adaptation of saccades

The cerebellum is critically involved in the adaptation mechanisms that maintain the accuracy of goal-directed acts such as saccadic eye movements. Two categories of saccades, each relying on different adaptation mechanisms, are defined: reactive (externally triggered) saccades and voluntary (internally triggered) saccades. The contribution of the medio-posterior part of the cerebellum to reactive saccades adaptation has been clearly demonstrated, but the evidence that other parts of the cerebellum are also involved is limited. Moreover, the cerebellar substrates of voluntary saccades adaptation have only been marginally investigated. Here, we addressed these two questions by investigating the adaptive capabilities of patients with cerebellar or pre-cerebellar stroke. We recruited three groups of patients presenting focal lesions located, respectively, in the supero-anterior cerebellum, the infero-posterior cerebellum and the lateral medulla (leading to a Wallenberg syndrome including motor dysfunctions similar to those resulting from lesion of the medio-posterior cerebellum). Adaptations of reactive saccades and of voluntary saccades were tested during separate sessions in all patients and in a group of healthy participants. The functional lesion of the medio-posterior cerebellum in Wallenberg syndrome strongly impaired the adaptation of both reactive and voluntary saccades. In contrast, patients with lesion in the supero-anterior part of the cerebellum presented a specific adaptation deficit of voluntary saccades. Finally, patients with an infero-posterior cerebellar lesion showed mild adaptation deficits. We conclude that the medio-posterior cerebellum is critical for the adaptation of both saccade categories, whereas the supero-anterior cerebellum is specifically involved in the adaptation of voluntary saccades.

A Role for the Parietal Cortex in Sensorimotor Adaptation of Saccades

Sensorimotor adaptation ensures movement accuracy despite continuously changing environment and body. Adaptation of saccadic eye movements is a classical model of sensorimotor adaptation. Beside the well-established role of the brainstem-cerebellum in the adaptation of reactive saccades (RSs), the cerebral cortex has been suggested to be involved in the adaptation of voluntary saccades (VSs). Here, we provide direct evidence for a causal involvement of the parietal cortex in saccadic adaptation. First, the posterior intraparietal sulcus (pIPS) was identified in each subject using functional magnetic resonance imaging (fMRI). Then, a saccadic adaptation paradigm was used to progressively reduce the amplitude of RSs and VSs, while single-pulse transcranial magnetic stimulation (spTMS) was applied over the right pIPS. The perturbations of pIPS resulted in impairment for the adaptation of VSs, selectively when spTMS was applied 60 ms after saccade onset. In contrast, the adaptation of RSs was facilitated by spTMS applied 90 ms after saccade initiation. The differential effect of spTMS relative to saccade types suggests a direct interference with pIPS activity for the VS adaptation and a remote interference with brainstem-cerebellum activity for the RS adaptation. These results support the hypothesis that the adaptation of VSs and RSs involves different neuronal substrates.

Functional activation of the cerebral cortex related to sensorimotor adaptation of reactive and voluntary saccades

Potentially dangerous events in the environment evoke automatic ocular responses, called reactive saccades. Adaptation processes, which maintain saccade accuracy against various events (e.g. growth, aging, neuro-muscular lesions), are to date mostly relayed to cerebellar activity. Here we demonstrate that adaptation of reactive saccades also involves cerebral cortical areas. Moreover, we provide the first identification of the neural substrates of adaptation of voluntary saccades, representing the complement to reactive saccades for the active exploration of our environment. An fMRI approach was designed to isolate adaptation from saccade production: an adaptation condition in which the visual target stepped backward 50 ms after saccade termination was compared to a control condition where the same target backstep occurred 500 ms after saccade termination. Subjects were tested for reactive and voluntary saccades in separate sessions. Multi-voxel pattern analyses of fMRI data from previously-defined regions of interests (ROIs) significantly discriminated between adaptation and control conditions for several ROIs. Some of these areas were revealed for adaptation of both saccade categories (cerebellum, frontal cortex), whereas others were specifically related to reactive saccades (temporo-parietal junction, hMT+/V5) or to voluntary saccades (medial and posterior areas of intra-parietal sulcus). These findings critically extend our knowledge on brain motor plasticity by showing that saccadic adaptation relies on a hitherto unknown contribution of the cerebral cortex.

Sensory Processing of Motor Inaccuracy Depends on Previously Performed Movement and on Subsequent Motor Corrections: A Study of the Saccadic System

When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.

Hand–eye coordination relies on extra-retinal signals: Evidence from reactive saccade adaptation

Execution of a saccadic eye movement towards the goal of a hand pointing movement improves the accuracy of this hand movement. Still controversial is the role of extra-retinal signals, i.e. efference copy of the saccadic command and/or ocular proprioception, in the definition of the hand pointing target. We report here that hand pointing movements produced without visual feedback, with accompanying saccades and towards a target extinguished at saccade onset, were modified after gain change of reactive saccades through saccadic adaptation. As we have previously shown that the adaptation of reactive saccades does not influence the target representations that are common to the eye and the hand motor sub-systems (Cotti J, Guillaume A, Alahyane N, Pelisson D, Vercher JL. Adaptation of voluntary saccades, but not of reactive saccades. Transfers to hand pointing movements. J Neurophysiol 2007;98:602–12), the results of the present study demonstrate that extra-retinal signals participate in defining the target of hand pointing movements.

Adaptation of reactive and voluntary saccades: different patterns of adaptation revealed in the antisaccade task

Sensorimotor adaptation restores and maintains the accuracy of goal-directed movements. It remains unclear whether these adaptive mechanisms modify actions by controlling peripheral premotor stages that send commands to the effectors and/or earlier processing stages involved in registration of target location. Here, we studied the effect of adaptation of saccadic eye movements, a well-established model of sensorimotor adaptation, in an antisaccade task. This task introduces a clear spatial dissociation between the actual target direction and the requested saccade direction because the correct movement direction is in the opposite direction from the target location. We used this requirement of a vector inversion to assess the level(s) of saccadic adaptation for two different types of adapted saccades. In two different experiments, we tested the transfer to antisaccades of the adaptation in one direction of reactive saccades to jumping targets and of scanning voluntary saccades within a target array. In the first experiment, we found that adaptation of reactive saccades transferred only to antisaccades in the adapted direction. In contrast, in the second experiment, adaptation of scanning voluntary saccades transferred to antisaccades in both the adapted and non-adapted directions. We conclude that adaptation of reactive saccades acts only downstream of the vector inversion required in the antisaccade task, whereas adaptation of voluntary saccades has a distributed influence, acting both upstream and downstream of vector inversion.

Adaptation of Voluntary Saccades, But Not of Reactive Saccades, Transfers to Hand Pointing Movements

Studying the transfer of visuomotor adaptation from a given effector (e.g., the eye) to another (e.g., the hand) allows us to question whether sensorimotor processes influenced by adaptation are common to both effector control systems and thus to address the level where adaptation takes place. Previous studies have shown only very weak transfer of the amplitude adaptation of reactive saccades--i.e., produced automatically in response to the sudden appearance of visual targets--to hand pointing movements. Here we compared the amplitude of hand pointing movements recorded before and after adaptation of either reactive or voluntary saccades, produced either in a saccade sequence task or in a single saccade task. No transfer to hand pointing movements was found after adaptation of reactive saccades. In contrast, a substantial transfer to the hand was obtained following adaptation of voluntary saccades produced in sequence. Large amounts of transfer between the two saccade types were also found. These results demonstrate that the visuomotor processes influenced by saccadic adaptation depend on the type of saccades and that, in the case of voluntary saccades, they are shared by hand pointing movements. Implications for the neurophysiological substrates of the adaptation of reactive and voluntary saccades are discussed.

Oculomotor plasticity: Are mechanisms of adaptation for reactive and voluntary saccades separate?

Saccadic eye movements are permanently controlled and their accuracy maintained by adaptive mechanisms that compensate for physiological or pathological perturbations. In contrast to the adaptation of reactive saccades (RS) which are automatically triggered by the sudden appearance of a single target, little is known about the adaptation of voluntary saccades which allow us to intentionally scan our environment in nearly all our daily activities. In this study, we addressed this issue in human subjects by determining the properties of adaptation of scanning voluntary saccades (SVS) and comparing these features to those of RS. We also tested the reciprocal transfers of adaptation between the two saccade types. Our results revealed that SVS and RS adaptations disclosed similar adaptation fields, time course and recovery levels, with only a slightly lower after-effect for SVS. Moreover, RS and SVS main sequences both remained unaffected after adaptation. Finally and quite unexpectedly, the pattern of adaptation transfers was asymmetrical, with a much stronger transfer from SVS to RS (79%) than in the reverse direction (22%). These data demonstrate that adaptations of RS and SVS share several behavioural properties but at the same time rely on partially distinct processes. Based on these findings, it is proposed that adaptations of RS and SVS may involve a neural network including both a common site and two separate sites specifically recruited for each saccade type.