Gaze Orienting in Dynamic Visual Double Steps Joyce Vliegen, Tom J. Van Grootel and A. John Van Opstal JN 94:4300-4313, 2005. First published Aug 17, 2005; doi:10.1152/jn.00027.2005 You might find this additional information useful... This article cites 55 articles, 16 of which you can access free at: http://jn.physiology.org/cgi/content/full/94/6/4300#BIBL Updated information and services including high-resolution figures, can be found at: http://jn.physiology.org/cgi/content/full/94/6/4300 Additional material and information about Journal of Neurophysiology can be found at: http://www.the-aps.org/publications/jn This information is current as of February 21, 2006 . Downloaded from jn.physiology.org on February 21, 2006 Journal of Neurophysiology publishes original articles on the function of the nervous system. It is published 12 times a year (monthly) by the American Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2005 by the American Physiological Society. ISSN: 0022-3077, ESSN: 1522-1598. Visit our website at http://www.the-aps.org/. J Neurophysiol 94: 4300–4313, 2005. First published August 17, 2005; doi:10.1152/jn.00027.2005. Gaze Orienting in Dynamic Visual Double Steps Joyce Vliegen, Tom J. Van Grootel, and A. John Van Opstal Department of Medical Physics and Biophysics, Radboud University Nijmegen, Nijmegen, The Netherlands Submitted 10 January 2005; accepted in final form 11 August 2005 Vliegen, Joyce, Tom J. Van Grootel, and A. John Van Op- and head (e.g., Goossens and Van Opstal 1997b). Instead, the stal. Gaze orienting in dynamic visual double steps. J Neuro- correct motor errors (TE,2 and TH,2, respectively) require dif- physiol 94: 4300–4313, 2005. First published August 17, 2005; ferent transformations of the target location that incorporate doi:10.1152/jn.00027.2005. Visual stimuli are initially represented both the eye–head misalignment and the intervening eye–head in a retinotopic reference frame. To maintain spatial accuracy of gaze movements. (i.e., eye in space) despite intervening eye and head movements, the visual input could be combined with dynamic feedback about ongoing The gaze control system could implement these transforma- gaze shifts. Alternatively, target coordinates could be updated in tions in a variety of ways. For example, it could use prepro- advance by using the preprogrammed gaze-motor command (“predic- grammed (feedforward) information about the upcoming gaze tive remapping”). So far, previous experiments have not dissociated shift. Alternatively, it could rely on continuous dynamic feed- these possibilities. Here we study whether the visuomotor system back about the actual movements of eyes and head. Downloaded from accounts for saccadic eye–head movements that occur during target To study these different transformations we have elicited presentation. In this case, the system has to deal with fast dynamic eye–head saccades to visual stimuli that were briefly flashed changes of the retinal input and with highly variable changes in during an intervening eye–head gaze shift. relative eye and head movements that cannot be preprogrammed by the gaze control system. We performed visual–visual double-step experiments in which a brief (50-ms) stimulus was presented during a Static double steps saccadic eye–head gaze shift toward a previously flashed visual Our paradigm contrasts with the classic saccade double-step jn.physiology.org target. Our results show that gaze shifts remain accurate under these experiment, which we here denote as the static double step dynamic conditions, even for stimuli presented near saccade onset, (Fig. 2A). In that experiment two peripheral targets are pre- and that eyes and head are driven in oculocentric and craniocentric coordinates, respectively. These results cannot be explained by a sented shortly after each other, but before the initiation of the predictive remapping scheme. We propose that the visuomotor system first gaze shift. The subject is instructed to foveate both targets adequately processes dynamic changes in visual input that result from at the remembered spatial locations in the order of their self-initiated gaze shifts, to construct a stable representation of visual appearance. The double-step paradigm has been used in a on February 21, 2006 targets in an absolute, supraretinal (e.g., world) reference frame. number of (head-fixed) saccadic eye-movement studies Predictive remapping may subserve transsaccadic integration, thus (Becker and Ju¨rgens 1979; Goossens and Van Opstal 1997a; enabling perception of a stable visual scene despite eye movements, Ottes et al. 1984), all of which showed that saccades toward the whereas dynamic feedback ensures accurate actions (e.g., eye–head second target fully account for the size and direction of the first orienting) to a selected goal. eye movement. Several theories to explain this result have been forwarded in the literature. INTRODUCTION Position versus displacement feedback This paper concerns the transformations underlying the pro- gramming of two-dimensional (2D) head-free gaze shifts to Neurophysiological studies have demonstrated that the pri- visual targets. Gaze is the orientation of the visual axis in mate visuomotor system also compensates for an intervening space, defined by the sum of the orientations of the eye in the saccade evoked by microstimulation of the midbrain superior head and the head in space. colliculus (SC; Mays and Sparks 1980; Sparks and Mays In studies of the gaze control system the typical situation is 1983). These studies suggested that the retinal location of the one in which eye and head orientations are initially aligned target is transformed into a head-centered reference frame, in (exceptions are, e.g., Goossens and Van Opstal 1997b; Stahl which the system can readily program the future saccade by 2001; Volle and Guitton 1993). Under such conditions, there is incorporating eye-in-head position (Sparks and Mays 1983; a one-to-one correspondence between the retinal location of a Van Gisbergen et al. 1981; Zipser and Andersen 1988). How- briefly flashed visual stimulus and the motor commands for ever, lack of evidence for a head-centered representation of eyes and head to acquire the target. However, under more visual targets, together with the idea that the SC represents natural conditions, the eyes are not fixed in the head. Eyes and saccades in an eye-centered, rather than in a head-centered head may then not point in the same direction, and make motor map (Robinson 1972; Sparks and Mays 1983), has different intervening movements before the orienting response. prompted others to propose an eye-displacement updating As illustrated in Fig. 1, in such cases the initial retinal error scheme to explain these results. In this scheme, the visuomotor system keeps targets in an eye-centered reference frame, while (TE,0) no longer suffices as a valid motor command for eyes updating the saccade plan with feedback about intervening eye Address for reprint requests and other correspondence: A. J. Van Opstal, Department of Medical Physics and Biophysics, Radboud University Nijme- The costs of publication of this article were defrayed in part by the payment gen, Geert Grooteplein 21, 6525 EZ Nijmegen, The Netherlands (E-mail: of page charges. The article must therefore be hereby marked “advertisement” [email protected]). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. 4300 0022-3077/05 $8.00 Copyright © 2005 The American Physiological Society www.jn.org DYNAMIC EYE–HEAD ORIENTING 4301 tion about eye and head movements through dynamic feedback from the gaze control system. In this way, the motor errors that will drive the eye and head are always accurate. The static double-step paradigm (Fig. 2A), in which both targets are presented before the eye–head movement onset, cannot dissociate updating schemes based on dynamic feed- back from those based on predictive remapping. Although the VP model predicts a localization error that depends on the error for the first target, both the MP and the FB models predict equally accurate localization responses. Dynamic double steps In the present study we have applied a dynamic double-step FIG. 1. In head-free gaze shifts, eye and head are typically unaligned, and paradigm, in which the second target is presented in midflight make movements of different amplitudes, thus creating different error signals ⌬ for a visual target. Scheme shows a fixation point (F), a first visual stimulus of the first, intervening gaze shift ( G1, Fig. 2B). If predictive ⌬ (V1), and a second visual target (V2), both presented before the eye ( G1) remapping would underlie the programming of the future gaze ⌬ –head ( H1) movement toward V1. At the start of the trial, the eye-in-head shift, systematic errors are expected in this paradigm (VP, MP position is E . Initial retinal error for V is T , but for the head it is different: 0 2 E,0 vectors) because, in these models, the system is supposed to TH,0. After the first gaze shift, the eye-in-head position has changed (E1) and update the initial retinal input on the basis of prior (i.e., Downloaded from the motor errors for eye (TE,2) and head (TH,2) are very different from the original retinal error, TE,0. They depend on the intervening eye–head gaze shift preprogrammed) information about the entire first gaze shift. ϭ Ϫ⌬ for the eye-in-space (TE,2 TE,0 G1) and on the eye–head misalignment According to the MP model, the target is missed by the ϭ ϩ Ϫ and head (or eye–head) movement for the head-in-space (TH,2 TE,0 E0 difference between the full gaze shift and the partial movement ⌬H ϭ T ϩ E Ϫ⌬G ), respectively. 1 E,0 1 1 after the onset of the second target, ⌬G*.