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      Frontal Eye Field Inactivation Diminishes Superior Colliculus Activity, But Delayed Saccadic Accumulation Governs Reaction Time Increases

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          Abstract

          Stochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEFs) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation by relating variations in saccade reaction time (SRT) to variations in such parameters as baseline, rate of accumulation of activity, and threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in four male nonhuman primates, we causally tested which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation.

          SIGNIFICANCE STATEMENT The superior colliculus (SC) and frontal eye fields (FEFs) are two of the best-studied areas in the primate brain. Surprisingly, little is known about what happens in the SC when the FEF is temporarily inactivated. Here, we show that temporary FEF inactivation decreases all aspects of functionally related activity in the SC. This combination of techniques also enabled us to relate changes in SC activity to concomitant increases in saccadic reaction time (SRT). Although stochastic accumulator models relate SRT increases to reduced rates of accumulation or increases in threshold, such changes were not observed in the SC. Instead, FEF inactivation delayed the onset of saccade-related accumulation, emphasizing the importance of this parameter in biologically plausible models of saccade initiation.

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          Author and article information

          Journal
          J Neurosci
          J. Neurosci
          jneuro
          jneurosci
          J. Neurosci
          The Journal of Neuroscience
          Society for Neuroscience
          0270-6474
          1529-2401
          29 November 2017
          : 37
          : 48
          : 11715-11730
          Affiliations
          [1] 1The Brain and Mind Institute,
          [2] 2Department of Physiology & Pharmacology,
          [3] 3Department of Psychology, and
          [4] 4Graduate Program in Neuroscience, University of Western Ontario, London, Ontario N6A 5B7, Canada, and
          [5] 5Robarts Research Institute, London, Ontario N6A 5K8, Canada
          Author notes
          Correspondence should be addressed to Dr. Brian D. Corneil, Robarts Research Institute, 1151 Richmond Street N, London, ON N6A 5B7, Canada. bcorneil@ 123456uwo.ca

          Author contributions: T.R.P., S.G.L., and B.D.C. designed research; T.R.P. and S.D. performed research; S.G.L. contributed unpublished reagents/analytic tools; T.R.P. and B.D.C. analyzed data; T.R.P., S.D., and B.D.C. wrote the paper.

          Author information
          http://orcid.org/0000-0002-4702-7089
          Article
          PMC6705743 PMC6705743 6705743 2664-17
          10.1523/JNEUROSCI.2664-17.2017
          6705743
          29089439
          a3f3c3a7-46c3-42ff-9db6-2ab65f8594d1
          Copyright © 2017 the authors 0270-6474/17/3711715-16$15.00/0
          History
          : 15 September 2017
          : 20 October 2017
          : 24 October 2017
          Categories
          Research Articles
          Systems/Circuits

          frontal eye fields,superior colliculus,saccade,reversible inactivation,computational models

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