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Research Articles, Behavioral/Cognitive

Stable Working Memory and Perceptual Representations in Macaque Lateral Prefrontal Cortex during Naturalistic Vision

Megan Roussy, Benjamin Corrigan, Rogelio Luna, Roberto A. Gulli, Adam J. Sachs, Lena Palaniyappan and Julio C. Martinez-Trujillo
Journal of Neuroscience 2 November 2022, 42 (44) 8328-8342; DOI: https://doi.org/10.1523/JNEUROSCI.0597-22.2022
Megan Roussy
1Department of Physiology and Pharmacology, Western University, London, Ontario N6A 5C1, Canada
2Robarts Research Institute, Western University, London, Ontario N6A 3K7, Canada
5Department of Psychiatry, McGill University, Montreal, Quebec H3A 1A1, Canada
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Benjamin Corrigan
1Department of Physiology and Pharmacology, Western University, London, Ontario N6A 5C1, Canada
2Robarts Research Institute, Western University, London, Ontario N6A 3K7, Canada
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Rogelio Luna
1Department of Physiology and Pharmacology, Western University, London, Ontario N6A 5C1, Canada
2Robarts Research Institute, Western University, London, Ontario N6A 3K7, Canada
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Roberto A. Gulli
3Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, New York 10027
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Adam J. Sachs
4The Ottawa Hospital, University of Ottawa, Ottawa, Ontario K1H 8L6, Canada
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Lena Palaniyappan
5Department of Psychiatry, McGill University, Montreal, Quebec H3A 1A1, Canada
6Centre for Youth Mental Health, Douglas Mental Health University Institute, Montreal, Quebec H4H 1R3, Canada
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Julio C. Martinez-Trujillo
1Department of Physiology and Pharmacology, Western University, London, Ontario N6A 5C1, Canada
2Robarts Research Institute, Western University, London, Ontario N6A 3K7, Canada
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Abstract

Primates use perceptual and mnemonic visuospatial representations to perform everyday functions. Neurons in the lateral prefrontal cortex (LPFC) have been shown to encode both of these representations during tasks where eye movements are strictly controlled and visual stimuli are reduced in complexity. This raises the question of whether perceptual and mnemonic representations encoded by LPFC neurons remain robust during naturalistic vision—in the presence of a rich visual scenery and during eye movements. Here we investigate this issue by training macaque monkeys to perform working memory and perception tasks in a visually complex virtual environment that requires navigation using a joystick and allows for free visual exploration of the scene. We recorded the activity of 3950 neurons in the LPFC (areas 8a and 9/46) of two male rhesus macaques using multielectrode arrays, and measured eye movements using video tracking. We found that navigation trajectories to target locations and eye movement behavior differed between the perception and working memory tasks, suggesting that animals used different behavioral strategies. Single neurons were tuned to target location during cue encoding and working memory delay, and neural ensemble activity was predictive of the behavior of the animals. Neural decoding of the target location was stable throughout the working memory delay epoch. However, neural representations of similar target locations differed between the working memory and perception tasks. These findings indicate that during naturalistic vision, LPFC neurons maintain robust and distinct neural codes for mnemonic and perceptual visuospatial representations.

SIGNIFICANCE STATEMENT We show that lateral prefrontal cortex neurons encode working memory and perceptual representations during a naturalistic task set in a virtual environment. We show that despite eye movement and complex visual input, neurons maintain robust working memory representations of space, which are distinct from neuronal representations for perception. We further provide novel insight into the use of virtual environments to construct behavioral tasks for electrophysiological experiments.

  • nonhuman primate
  • prefrontal cortex
  • visual perception
  • working memory

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The Journal of Neuroscience: 42 (44)
Journal of Neuroscience
Vol. 42, Issue 44
2 Nov 2022
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Stable Working Memory and Perceptual Representations in Macaque Lateral Prefrontal Cortex during Naturalistic Vision
Megan Roussy, Benjamin Corrigan, Rogelio Luna, Roberto A. Gulli, Adam J. Sachs, Lena Palaniyappan, Julio C. Martinez-Trujillo
Journal of Neuroscience 2 November 2022, 42 (44) 8328-8342; DOI: 10.1523/JNEUROSCI.0597-22.2022

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Stable Working Memory and Perceptual Representations in Macaque Lateral Prefrontal Cortex during Naturalistic Vision
Megan Roussy, Benjamin Corrigan, Rogelio Luna, Roberto A. Gulli, Adam J. Sachs, Lena Palaniyappan, Julio C. Martinez-Trujillo
Journal of Neuroscience 2 November 2022, 42 (44) 8328-8342; DOI: 10.1523/JNEUROSCI.0597-22.2022
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Keywords

  • nonhuman primate
  • prefrontal cortex
  • visual perception
  • working memory

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