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      Transient Pupil Dilation after Subsaccadic Microstimulation of Primate Frontal Eye Fields

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          Abstract

          Pupillometry provides a simple and noninvasive index for a variety of cognitive processes, including perception, attention, task consolidation, learning, and memory. The neural substrates by which such cognitive processes influence pupil diameter remain somewhat unclear, although cortical inputs to the locus coeruleus mediating arousal are likely involved. Changes in pupil diameter also accompany covert orienting; hence the oculomotor system may provide an alternative substrate for cognitive influences on pupil diameter. Here, we show that low-level electrical microstimulation of the primate frontal eye fields (FEFs), a cortical component of the oculomotor system strongly connected to the intermediate layers of the superior colliculus (SCi), evoked robust pupil dilation even in the absence of evoked saccades. The magnitude of such dilation scaled with increases in stimulation parameters, depending strongly on the intensity and number of pulses. Although there are multiple pathways by which FEF stimulation could cause pupil dilation, the timing and profile of dilation closely resembled that evoked by SCi stimulation. Moreover, pupil dilation evoked from the FEFs increased when presumed oculomotor activity was higher at the time of stimulation. Our findings implicate the oculomotor system as a potential substrate for how cognitive processes can influence pupil diameter. We suggest that a pathway from the frontal cortex through the SCi operates in parallel with frontal inputs to arousal circuits to regulate task-dependent modulation of pupil diameter, perhaps indicative of an organization wherein one pathway assumes primacy for a given cognitive process.

          SIGNIFICANCE STATEMENT Pupillometry (the measurement of pupil diameter) provides a simple and noninvasive index for a variety of cognitive processes, offering a biomarker that has value in both health and disease. But how do cognitive processes influence pupil diameter? Here, we show that low-level stimulation of the primate frontal eye fields can induce robust pupil dilation without saccades. Pupil dilation scaled with the number and intensity of stimulation pulses and varied with endogenous oculomotor activity at the time of stimulation. The oculomotor system therefore provides a plausible pathway by which cognitive processes may influence pupil diameter, perhaps operating in conjunction with systems regulating arousal.

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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
          30 March 2016
          : 36
          : 13
          : 3765-3776
          Affiliations
          [1] 1Departments of Physiology and Pharmacology and
          [2] 2Psychology, Western University, London, Ontario N6A 5B7, Canada and
          [3] 3The Brain and Mind Institute, Robarts Research Institute, London, Ontario N6A 5B7, Canada
          Author notes
          Correspondence should be addressed to Brian D. Corneil, Robarts Research Institute, London, Ontario N6A 5B7, Canada. E-mail: bcorneil@ 123456uwo.ca

          Author contributions: S.J.L. and B.D.C. designed research; S.J.L. performed research; S.J.L. analyzed data; S.J.L. and B.D.C. wrote the paper.

          Author information
          http://orcid.org/0000-0002-4702-7089
          Article
          PMC6601743 PMC6601743 6601743 4264-15
          10.1523/JNEUROSCI.4264-15.2016
          6601743
          27030761
          b4e4e206-c9bb-485b-837f-ecb5d73d5148
          Copyright © 2016 the authors 0270-6474/16/363765-12$15.00/0
          History
          : 26 November 2015
          : 12 February 2016
          : 25 February 2016
          Categories
          Articles
          Behavioral/Cognitive

          stimulation,pupil,oculomotor,monkey,frontal eye fields
          stimulation, pupil, oculomotor, monkey, frontal eye fields

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