Elsevier

Brain Research

Volume 1135, 2 March 2007, Pages 107-121
Brain Research

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

https://doi.org/10.1016/j.brainres.2006.11.077Get rights and content

Abstract

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.

Introduction

Saccadic eye movements are rapid and accurate shifts of the eyes which are permanently called for in our everyday life to gather visual information from our environment. Two main types of saccades can be distinguished (Tusa et al., 1986): voluntary (or intentional) saccades (VS) and reactive saccades (RS). VS are internally triggered toward permanent visual targets whereas RS are externally triggered by the sudden appearance of a novel visual target. The generation of these two types of saccades relies on two partially separate pathways, involving the frontal cortex and the occipito-parietal cortex for VS and RS, respectively (for reviews Pierrot-Deseilligny et al., 1991, Pierrot-Deseilligny et al., 2004, Tehovnik et al., 2000, Gaymard et al., 2003). In everyday life, we usually produce a specific type of voluntary saccades to explore complex visual scenes like a landscape or a page of reading. In this paper, we will focus on this type of intentionally generated saccades and will refer to them as scanning voluntary saccades (SVS).

Keeping an optimal performance of all these saccadic responses is critical for most of our sensory–motor and cognitive activities. It is known for nearly 30 years that adaptation mechanisms maintain saccade accuracy despite physiological or pathological perturbation of the sensory–motor saccadic system or of the relationship between this system and our environment. This saccadic adaptation phenomenon has been clearly revealed in patients and in monkeys with weakened extraocular muscles (Kommerell et al., 1976, Abel et al., 1978, Optican and Robinson, 1980). It can also be experimentally induced in healthy subjects by using the non-invasive double-step target paradigm first reported by McLaughlin (1967). This protocol consists of displacing a visual target to elicit a visually triggered saccade and then, during this primary saccade, of displacing the target again to yield a post-saccadic error. Repeated iterations of these double-step trials lead adaptive mechanisms to progressively adjust the saccade amplitude and to decrease the post-saccadic error. Using this protocol, the large majority of studies have so far focussed on the adaptation of RS (see for review Hopp and Fuchs, 2004). First, adaptation of a single RS transfers to other saccades of different amplitude and/or direction, provided their vector terminates in a restricted region called the “adaptation field” (Frens and Van Opstal, 1994). Inside the adaptation field, the amount of transfer monotonically decreases as the vector separation between the non-trained and the adapted saccade increases (Miller et al., 1981, Deubel, 1987, Frens and Van Opstal, 1994, Albano, 1996, Straube et al., 1997, Noto et al., 1999, Watanabe et al., 2000). These adaptation fields suggest that the neural locus (loci) where oculomotor commands are modified during RS adaptation encode(s) the saccadic vector (eye displacement signal), rather than the saccade goal (eye position signal). Second, the adaptation of RS involves the medio-posterior part of the cerebellum (vermis and fastigial nuclei), as revealed by imaging (Desmurget et al., 1998) and clinical studies (Straube et al., 2001) in man, and by lesion studies in monkey (Optican and Robinson, 1980, Goldberg et al., 1993, Takagi et al., 1998, Barash et al., 1999). Note however that it cannot be excluded that at least part of RS adaptation occurs upstream from the cerebellum, as suggested by a recent unit activity recording study in the nucleus reticularis tegmenti pontis (NRTP) in monkeys (Takeichi et al., 2005). In addition to the cerebellum, converging evidence suggests that the main site of adaptation-related modification of motor commands lies in the brainstem, possibly at the level of – or downstream from – the superior colliculus (Kröller et al., 1996, Kröller et al., 1999, Melis and Van Gisbergen, 1996, Frens and Van Opstal, 1997, Deubel, 1999, Edelman and Goldberg, 2002, Hopp and Fuchs, 2002, Alahyane et al., 2004). This site was further clarified by our previous study (Alahyane and Pélisson, 2005) which demonstrated that the large adaptive modification of RS amplitude was not accompanied by any change in the main sequence relationship (peak velocity versus amplitude). This finding suggested that the plastic neuronal modifications which underlie the adaptation of RS do not include the brainstem saccadic pulse generator.

By comparison to this growing knowledge of RS adaptation, the neural substrate and behavioural properties of adaptation of VS remain very little known. Yet VS, particularly SVS, represent the most common type of saccades in everyday life. Moreover, since SVS and RS are generated by different neural circuits, it is quite possible that the neural processes of adaptation and resulting behavioural properties largely differ between these two types of saccades. Thus the knowledge of RS adaptation summarized above cannot, a priori, be extrapolated to SVS adaptation. It is therefore crucial to specifically investigate the mechanisms underlying adaptation of SVS. Besides, some previous studies showed no or limited transfer of adaptation between RS and VS in human, suggesting that the neural mechanisms controlling adaptation of these two types of saccades are separated (Erkelens and Hulleman, 1993, Deubel, 1995, Fujita et al., 2002, Collins and Dore-Mazars, 2006). However, cautions have to be taken since these prior works have not all dealt with the same sub-type of VS and have not always measured the adaptation after-effect that allows quantification of the true adaptation level, independently of non-specific factors. Indeed, studies of RS have shown the existence of a rapid drop of adaptation-related gain change between the end of the adaptation session and the subsequent test session (Straube et al., 1997, Scudder et al., 1998, Alahyane and Pélisson, 2005). A similar gain drop cannot a priori, be rejected for VS, which could have a strong impact on the computation of the transfer of VS adaptation to RS. Another behavioural study (Gaveau et al., 2005) revealed that the adaptively modified gain of RS does not recover when subjects perform VS to stationary targets during a 15-min “de-adaptation” period. These results suggest thus that VS de-adaptation and RS adaptation rely on separate mechanisms. But here again, cautions have to be taken since it is still debated whether or not de-adaptation and adaptation rely on similar mechanisms. As a final note, the neural substrate of SVS adaptation has never been explored.

The present work was thus aimed at determining the properties of SVS adaptation and at testing to what extent RS and SVS adaptations differ in healthy human subjects. We focussed on the search for adaptation fields and saccade dynamics changes in SVS adaptation. We also measured the transfer of adaptation between SVS and RS. These features are potentially quite informative about the neural substrates underlying adaptations of SVS and RS. Two main possibilities can be envisioned. First, if adaptations of SVS and RS rely on completely separated processes, we expect very low values of adaptation transfer between the two saccade types. Adaptation properties however would be either different or similar. Conversely, if adaptations of SVS and RS rely on a common process, then the adaptation properties should be very similar and the adaptation transfer high and symmetrical. Part of data has been reported in an abstract form (Pélisson et al., 2005).

Section snippets

Results

The two saccade types (RS and SVS) were tested in two separate experiments (see Fig. 1). In each experiment, rightward and leftward saccades towards 8° eccentric targets were simultaneously adapted. In the RS experiment, the classical double-step target protocol was used to reduce the RS amplitude by systematically displacing the visual target backward during the primary saccade. In the SVS experiment, subjects performed a series of 3 horizontal SVS during the exploration of a set of 4

Discussion

The main objective of the present study was to test whether adaptation of scanning voluntary saccades (SVS) is a separate process from adaptation of reactive saccades (RS). To this aim, we compared their functional properties, and found that many of them were similar: i) adaptation is incomplete, as seen by the saturating time course of amplitude changes and by the limitation of after-effect to 39% (48.5% for RS) of the final intra-saccadic target displacement, ii) it may be subjected to fast

Subjects

The experiment was conducted in six participants (3 authors; age 22–48 years). All subjects had a normal or a corrected to normal vision and provided their informed consent before the recording sessions. The study complied with the declaration of Helsinki.

Apparatus

Participants were sitting in a dimly illuminated room with their head stabilized by a chin rest and a cheekbone rest, facing a fast video screen controlled by a VSG (Visual Stimuli Generation) system (CR, Cambridge, UK). They were required to

Acknowledgments

We thank all the subjects for their kind participation in the present study. We also thank P. Vindras, P. Baraduc and V. Fonteille for useful discussions. We are also grateful to J.L. Borach for his assistance in figure preparation. Experiments were performed in the “Mouvement et Handicap” IFNL platform (Lyon, France) and were approved by the local Ethic committee (CCPPRB-Lyon B). This work was funded by a grant from the Fondation pour la Recherche Médicale (N. Alahyane) and the French

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