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New Research, Sensory and Motor Systems

Binocular suppression in the macaque lateral geniculate nucleus reveals early competitive interactions between the eyes

Kacie Dougherty, Brock M. Carlson, Michele A. Cox, Jacob A. Westerberg, Wolf Zinke, Michael C. Schmid, Paul R. Martin and Alexander Maier
eNeuro 25 January 2021, ENEURO.0364-20.2020; DOI: https://doi.org/10.1523/ENEURO.0364-20.2020
Kacie Dougherty
1Department of Psychology, College of Arts and Science, Vanderbilt Vision Research Center, Center for Integrative and Cognitive Neuroscience, Vanderbilt University, Nashville, TN 37235, USA
2Princeton Neuroscience Institute, Princeton University, Princeton, NJ 09540, USA
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Brock M. Carlson
1Department of Psychology, College of Arts and Science, Vanderbilt Vision Research Center, Center for Integrative and Cognitive Neuroscience, Vanderbilt University, Nashville, TN 37235, USA
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Michele A. Cox
1Department of Psychology, College of Arts and Science, Vanderbilt Vision Research Center, Center for Integrative and Cognitive Neuroscience, Vanderbilt University, Nashville, TN 37235, USA
3Department of Brain and Cognitive Sciences, University of Rochester, Rochester, NY 14620, USA
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Jacob A. Westerberg
1Department of Psychology, College of Arts and Science, Vanderbilt Vision Research Center, Center for Integrative and Cognitive Neuroscience, Vanderbilt University, Nashville, TN 37235, USA
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Wolf Zinke
1Department of Psychology, College of Arts and Science, Vanderbilt Vision Research Center, Center for Integrative and Cognitive Neuroscience, Vanderbilt University, Nashville, TN 37235, USA
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Michael C. Schmid
4Faculty of Science and Medicine, University of Fribourg, Chemin du Musée 5 CH-1700 Fribourg, Switzerland
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Paul R. Martin
5Save Sight Institute and Australian Research Council Centre of Excellence for Integrative Brain Function, The University of Sydney, Sydney, New South Wales 2006, Australia
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Alexander Maier
1Department of Psychology, College of Arts and Science, Vanderbilt Vision Research Center, Center for Integrative and Cognitive Neuroscience, Vanderbilt University, Nashville, TN 37235, USA
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Abstract

The lateral geniculate nucleus (LGN) of the dorsal thalamus is the primary recipient of the two eyes’ outputs. Most LGN neurons are monocular in that they are activated by visual stimulation through only one (dominant) eye. However, there are both intrinsic connections and inputs from binocular structures to the LGN that could provide these neurons with signals originating from the other (non-dominant) eye. Indeed, previous work introducing luminance differences across the eyes or using a single-contrast stimulus showed binocular modulation for single unit activity in anesthetized macaques and multiunit activity in awake macaques. Here, we sought to determine the influence of contrast viewed by both the non-dominant and dominant eyes on LGN single-unit responses in awake macaques. To do this, we adjusted each eye’s signal strength by independently varying the contrast of stimuli presented to the two eyes. Specifically, we recorded LGN single unit spiking activity in two awake macaques while they viewed drifting gratings of varying contrast. We found that LGN neurons of all types (parvo-, magno-, and koniocellular) were significantly suppressed when stimuli were presented at low contrast to the dominant eye and at high contrast to the non-dominant eye. Further, the inputs of the two eyes showed antagonistic interaction, whereby the magnitude of binocular suppression diminished with high contrast in the dominant eye, or low contrast in the non-dominant eye. These results suggest that the LGN represents a site of pre-cortical binocular processing involved in resolving discrepant contrast differences between the eyes.

Significance A fundamental feature of the primate visual system is its binocular arrangement, which affords stereovision and hyperacuity. A consequence of this arrangement is that the two eyes’ views need to be resolved to yield singular vision, which is normally accomplished by fusion or suppression of one of the eye’s inputs. This binocular processing has been shown to occur in cortex, subsequent to thalamic processing. Here, we show that neurons in the lateral geniculate nucleus receiving excitatory retinal input from one eye can be suppressed by high-contrast visual stimulation of the other eye, indicating that the geniculate serves as a pre-cortical site of binocular processing.

  • binocular
  • interocular suppression
  • lateral geniculate nucleus
  • macaque
  • monocular
  • vision

Footnotes

  • The authors report no conflicts of interest.

  • Supported by a research grant from the National Eye Institute (1R01EY027402-03) and National Eye Institute Training Grant (5T32EY007135-23) to JAW and K.D, National Institute of Mental Health Training Grant (5T32MH065214-17) to K.D, and National Eye Institute Training Grant (1F31EY031293-22) to J.A.W. M.C.S. is supported by ERC grant OptoVision 637638.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Binocular suppression in the macaque lateral geniculate nucleus reveals early competitive interactions between the eyes
Kacie Dougherty, Brock M. Carlson, Michele A. Cox, Jacob A. Westerberg, Wolf Zinke, Michael C. Schmid, Paul R. Martin, Alexander Maier
eNeuro 25 January 2021, ENEURO.0364-20.2020; DOI: 10.1523/ENEURO.0364-20.2020

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Binocular suppression in the macaque lateral geniculate nucleus reveals early competitive interactions between the eyes
Kacie Dougherty, Brock M. Carlson, Michele A. Cox, Jacob A. Westerberg, Wolf Zinke, Michael C. Schmid, Paul R. Martin, Alexander Maier
eNeuro 25 January 2021, ENEURO.0364-20.2020; DOI: 10.1523/ENEURO.0364-20.2020
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Keywords

  • binocular
  • interocular suppression
  • lateral geniculate nucleus
  • macaque
  • monocular
  • vision

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