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      Effects of Initial Eye Position on Saccades Evoked by Microstimulation in the Primate Superior Colliculus: Implications for Models of the SC Read-Out Process

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          Abstract

          The motor layers of the superior colliculus (SC) are thought to specify saccade amplitude and direction, independent of initial eye position. However, recent evidence suggests that eye position can modulate the level of activity of SC motor neurons. In this study, we tested whether initial eye position has an effect on microstimulation-evoked saccade amplitude. High (>300 Hz) and low (<300 Hz) frequency microstimulation was applied to 30 sites in the rostral part of the SC of two monkeys while they fixated one of six different locations. We found that the amplitude of the evoked saccades decreased with more contralateral initial eye positions. This effect was more pronounced in low frequency- compared to high frequency-evoked saccades, although it was present for both. Replication of these findings in head-free experiments showed that the effect of initial eye position was not due to physical constraints imposed by the oculomotor range. In addition to the effect of eye position on saccade amplitude, we also observed an increase in saccade latency and a decrease in the probability that microstimulation would evoke a saccade for low frequency stimulation at more contralateral eye positions. These findings suggest that an eye position signal can contribute to the read-out of the SC. Models of the saccadic pulse-step generator may need revision to incorporate an eye position modulation at the input stage.

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          Most cited references58

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          The main sequence, a tool for studying human eye movements

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            Eye movements evoked by collicular stimulation in the alert monkey.

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              Population coding of saccadic eye movements by neurons in the superior colliculus.

              The deeper layers of the superior colliculus are involved in the initiation and execution of saccadic (high velocity) eye movements. A large population of coarsely tuned collicular neurons is active before each saccade. The mechanisms by which the signals that precisely control the direction and amplitude of a saccade are extracted from the activity of the population are unknown. It has been assumed that the exact trajectory of a saccade is determined by the activity of the entire population and that information is not extracted from only the most active cells in the population at a subsequent stage of neural processing. The trajectory of a saccade could be based on vector summation of the movement tendencies provided by each member of the population of active neurons or be determined by a weighted average of the vector contributions of each neuron in the active population. Here we present the results of experiments in which a small subset of the active population was reversibly deactivated with lidocaine. These results are consistent with the predictions of the latter population-averaging hypothesis and support the general idea that the direction, amplitude and velocity of saccadic eye movements are based on the responses of the entire population of cells active before a saccadic eye movement.
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                Author and article information

                Journal
                Front Integr Neurosci
                Front. Integr. Neurosci.
                Frontiers in Integrative Neuroscience
                Frontiers Research Foundation
                1662-5145
                20 October 2010
                19 January 2011
                2010
                : 4
                : 130
                Affiliations
                [1] 1simpleCenter for Cognitive Neuroscience, Duke University Durham, NC, USA
                [2] 2simpleDepartment of Neurobiology, Duke University Durham, NC, USA
                [3] 3simpleDepartment of Psychology and Neuroscience, Duke University Durham, NC, USA
                Author notes

                Edited by: Elizabeth B. Torres, Rutgers University, USA

                Reviewed by: Raj Gandhi, University of Pittsburgh, USA; Mark A. Segraves, Northwestern University, USA; Michael Campos, Massachusetts General Hospital/Harvard Medical School, USA

                *Correspondence: Jennifer M. Groh, Center for Cognitive Neuroscience, Duke University, B203 Levine Sciences Research Building, Durham, NC 27708, USA. e-mail: jmgroh@ 123456duke.edu
                Article
                10.3389/fnint.2010.00130
                3025650
                21267431
                be144323-6738-4f9c-b47c-86ea075f4105
                Copyright © 2011 Groh.

                This is an open-access article subject to an exclusive license agreement between the authors and Frontiers Media SA, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

                History
                : 22 September 2010
                : 28 December 2010
                Page count
                Figures: 11, Tables: 1, Equations: 2, References: 60, Pages: 16, Words: 10902
                Categories
                Neuroscience
                Original Research

                Neurosciences
                pulse-step generator,reference frame,monkey,oculomotor,superior colliculus,eye position
                Neurosciences
                pulse-step generator, reference frame, monkey, oculomotor, superior colliculus, eye position

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