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Electrical stimulation of rhesus monkey nucleus reticularis gigantocellularis

II. Effects on metrics and kinematics of ongoing gaze shifts to visual targets

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Abstract

Saccade kinematics are altered by ongoing head movements. The hypothesis that a head movement command signal, proportional to head velocity, transiently reduces the gain of the saccadic burst generator (Freedman 2001, Biol Cybern 84:453–462) can account for this observation. Using electrical stimulation of the rhesus monkey nucleus reticularis gigantocellularis (NRG) to alter the head contribution to ongoing gaze shifts, two critical predictions of this gaze control hypothesis were tested. First, this hypothesis predicts that activation of the head command pathway will cause a transient reduction in the gain of the saccadic burst generator. This should alter saccade kinematics by initially reducing velocity without altering saccade amplitude. Second, because this hypothesis does not assume that gaze amplitude is controlled via feedback, the added head contribution (produced by NRG stimulation on the side ipsilateral to the direction of an ongoing gaze shift) should lead to hypermetric gaze shifts. At every stimulation site tested, saccade kinematics were systematically altered in a way that was consistent with transient reduction of the gain of the saccadic burst generator. In addition, gaze shifts produced during NRG stimulation were hypermetric compared with control movements. For example, when targets were briefly flashed 30° from an initial fixation location, gaze shifts during NRG stimulation were on average 140% larger than control movements. These data are consistent with the predictions of the tested hypothesis, and may be problematic for gaze control models that rely on feedback control of gaze amplitude, as well as for models that do not posit an interaction between head commands and the saccade burst generator.

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Notes

  1. Data were collected at an additional 15 sites, but at these sites fewer than 10 trials occurred in which stimulation onset was within the 0–50 ms range. These sites are not included in the table. However, results at these sites were qualitatively similar to data presented.

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Acknowledgements

This work is supported in part by the following grants NEI (US National Eye Institute) RO1-EY13239, and NSF (US National Science Foundation) IBN-0132335. E.G.F. is an Alfred P. Sloan Research Fellow. The authors thank Dr. Stanislaw Sobotka, Aaron Cecala, and anonymous reviewers for their comments on a previous version of the manuscript, G. Parker for technical support, and Dr. David Sparks for insightful comments on this and other research.

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  1. Department of Neurobiology and Anatomy, University of Rochester, 601 Elmwood Ave., Box 603, Rochester, NY 14642, USA

    Edward G. Freedman & Stephan Quessy

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  1. Edward G. Freedman
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Correspondence to Edward G. Freedman.

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Freedman, E.G., Quessy, S. Electrical stimulation of rhesus monkey nucleus reticularis gigantocellularis. Exp Brain Res 156, 357–376 (2004). https://doi.org/10.1007/s00221-004-1840-2

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