Journal of Neurophysiology, Vol 76, Issue 3 1744-1758, Copyright © 1996 by APS

ARTICLES

Short-term adaptation of electrically induced saccades in monkey superior colliculus

B. J. Melis and J. A. van Gisbergen
Department of Medical Physics and Biophysics, University of Nijmegen, The Netherlands.

1. This study focuses on the neural mechanisms underlying short-term adaptation of saccadic eye movements in the rhesus monkey. Involuntary saccades of various amplitudes and directions (E-saccades) were elicited in complete darkness by electrical stimulation (< or = 50 microA) in the deeper layers of the superior colliculus (SC) at 30 different sites in two monkeys. E-saccades at a given site could be adapted by presenting a visual target at a small distance from the expected end point immediately after their occurrence. The monkeys were trained to null the ensuing error signal by making the appropriate correction saccade to the visual target in many successive trials (E-adap paradigm). By properly adjusting the location of the visual target relative to the end point of the E-saccade, the latter could be modified in amplitude as well as in direction. 2. E-saccade modifications were highly significant, always in the intended direction, and occurred only if a postsaccadic visual error signal was created. These changes were plastic and required a subsequent E-adap series with an opposite error signal to cancel them. Their time course, both during the adaptation and the readaptation period, indicated that the modification was a slow and gradual process, as has been observed earlier in classical visual adaptation experiments. 3. Postadaptation tests, assessing whether the adaptation of E-saccades was also noticeable in normal visually guided saccades (V-saccades), showed incomplete adaptation transfer that was significant in most cases. A similar result, significant in all cases, was obtained with an extended version of the E-adap paradigm in which movement planning on the basis of target selection was possible. In this case, a presaccadic visual target was presented at the expected end point of the E-saccade, which was evoked just before the monkey would make a voluntary saccade itself (VE-adap). 4. In another series of experiments, V-saccades, which were matched to the optimal saccade vector of the particular collicular site under investigation, were adapted with the classical intrasaccadic target shift paradigm (V-adap). In agreement with earlier findings, this V-adaptation showed no transfer to the E-saccades. This result was obtained even in trials in which movement planning on the basis of target selection was possible (VE-test). 5. Our experiments have shown that saccades of collicular origin can be adapted and that presaccadic target selection is not crucial for this process. Both results are nicely in line with an existing model featuring a downstream adaptive corrector with access to SC inputs. This scheme, however, does not explain why the degree of saccadic adaptation, achieved by applying any of the three adaptation paradigms (E-adap, EV-adap, or V-adap), was never equally expressed in V- and E-saccades. Arguments for extending the model by adding a cortical input from the frontal eye fields to the adaptive corrector are discussed.

This article has been cited by other articles:

				M. Panouilleres, T. Weiss, C. Urquizar, R. Salemme, D. P. Munoz, and D. Pelisson Behavioral Evidence of Separate Adaptation Mechanisms Controlling Saccade Amplitude Lengthening and Shortening J Neurophysiol, March 1, 2009; 101(3): 1550 - 1559. [Abstract] [Full Text] [PDF]

				A. L. Cecala and E. G. Freedman Head-Unrestrained Gaze Adaptation in the Rhesus Macaque J Neurophysiol, January 1, 2009; 101(1): 164 - 183. [Abstract] [Full Text] [PDF]

				N. Takeichi, C. R. S. Kaneko, and A. F. Fuchs Activity Changes in Monkey Superior Colliculus During Saccade Adaptation J Neurophysiol, June 1, 2007; 97(6): 4096 - 4107. [Abstract] [Full Text] [PDF]

				M. Campos, A. Cherian, and M. A. Segraves Effects of Eye Position upon Activity of Neurons in Macaque Superior Colliculus J Neurophysiol, January 1, 2006; 95(1): 505 - 526. [Abstract] [Full Text] [PDF]

				N. Takeichi, C.R.S. Kaneko, and A. F. Fuchs Discharge of Monkey Nucleus Reticularis Tegmenti Pontis Neurons Changes During Saccade Adaptation J Neurophysiol, September 1, 2005; 94(3): 1938 - 1951. [Abstract] [Full Text] [PDF]

				N. L. Port and R. H. Wurtz Sequential Activity of Simultaneously Recorded Neurons in the Superior Colliculus During Curved Saccades J Neurophysiol, September 1, 2003; 90(3): 1887 - 1903. [Abstract] [Full Text] [PDF]

				M. Tanaka Contribution of Signals Downstream From Adaptation to Saccade Programming J Neurophysiol, September 1, 2003; 90(3): 2080 - 2086. [Abstract] [Full Text] [PDF]

				A. D. Van Beuzekom and J.A.M. Van Gisbergen Interaction Between Visual and Vestibular Signals for the Control of Rapid Eye Movements J Neurophysiol, July 1, 2002; 88(1): 306 - 322. [Abstract] [Full Text] [PDF]

				A. D. Van Beuzekom and J.A.M. Van Gisbergen Collicular Microstimulation During Passive Rotation Does Not Generate Fixed Gaze Shifts J Neurophysiol, June 1, 2002; 87(6): 2946 - 2963. [Abstract] [Full Text] [PDF]

				J. A. Edelman and M. E. Goldberg Effect of Short-Term Saccadic Adaptation on Saccades Evoked by Electrical Stimulation in the Primate Superior Colliculus J Neurophysiol, April 1, 2002; 87(4): 1915 - 1923. [Abstract] [Full Text] [PDF]

				A. D. Van Beuzekom and J.A.M. Van Gisbergen Properties of the Internal Representation of Gravity Inferred From Spatial-Direction and Body-Tilt Estimates J Neurophysiol, July 1, 2000; 84(1): 11 - 27. [Abstract] [Full Text] [PDF]

				H.H.L.M. Goossens and A. J. Van Opstal Blink-Perturbed Saccades in Monkey. I. Behavioral Analysis J Neurophysiol, June 1, 2000; 83(6): 3411 - 3429. [Abstract] [Full Text] [PDF]

				C. T. Noto, S. Watanabe, and A. F. Fuchs Characteristics of Simian Adaptation Fields Produced by Behavioral Changes in Saccade Size and Direction J Neurophysiol, June 1, 1999; 81(6): 2798 - 2813. [Abstract] [Full Text] [PDF]

				V. Chaturvedi and J. A. M. van Gisbergen Perturbation of Combined Saccade-Vergence Movements by Microstimulation in Monkey Superior Colliculus J Neurophysiol, May 1, 1999; 81(5): 2279 - 2296. [Abstract] [Full Text] [PDF]

				M. Takagi, D. S. Zee, and R. J. Tamargo Effects of Lesions of the Oculomotor Vermis on Eye Movements in Primate: Saccades J Neurophysiol, October 1, 1998; 80(4): 1911 - 1931. [Abstract] [Full Text] [PDF]

				C. A. Scudder, E. Y. Batourina, and G. S. Tunder Comparison of Two Methods of Producing Adaptation of Saccade Size and Implications for the Site of Plasticity J Neurophysiol, February 1, 1998; 79(2): 704 - 715. [Abstract] [Full Text] [PDF]

				J. O. Phillips, A. F. Fuchs, L. Ling, Y. Iwamoto, and S. Votaw Gain Adaptation of Eye and Head Movement Components of Simian Gaze Shifts J Neurophysiol, November 1, 1997; 78(5): 2817 - 2821. [Abstract] [Full Text] [PDF]

				H.H.L.M. Goossens and A. J. V. Opstal Local Feedback Signals Are Not Distorted By Prior Eye Movements: Evidence From Visually Evoked Double Saccades J Neurophysiol, July 1, 1997; 78(1): 533 - 538. [Abstract] [Full Text] [PDF]