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Flexible neural coding in sensory, parietal, and frontal cortices during goal-directed virtual navigation

View ORCID ProfileJean-Paul Noel, Edoardo Balzani, Eric Avila, Kaushik Lakshminarasimhan, Stefania Bruni, Panos Alefantis, Cristina Savin, Dora E. Angelaki
doi: https://doi.org/10.1101/2021.10.22.465526
Jean-Paul Noel
1Center for Neural Science, New York University, New York City, NY, USA
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Edoardo Balzani
1Center for Neural Science, New York University, New York City, NY, USA
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Eric Avila
1Center for Neural Science, New York University, New York City, NY, USA
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Kaushik Lakshminarasimhan
1Center for Neural Science, New York University, New York City, NY, USA
2Center for Theoretical Neuroscience, Columbia University, New York City, NY, USA
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Stefania Bruni
1Center for Neural Science, New York University, New York City, NY, USA
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Panos Alefantis
1Center for Neural Science, New York University, New York City, NY, USA
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Cristina Savin
1Center for Neural Science, New York University, New York City, NY, USA
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Dora E. Angelaki
1Center for Neural Science, New York University, New York City, NY, USA
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  • For correspondence: Da93@nyu.edu
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Abstract

We do not understand how neural nodes operate within the recurrent action-perception loops that characterize naturalistic self-environment interactions, nor how brain networks reconfigure during changing computational demands. Here, we record local field potentials (LFPs) and spiking activity simultaneously from the dorsomedial superior temporal area (MSTd), parietal area 7a, and dorsolateral prefrontal cortex (dlPFC) as monkeys navigate in virtual reality to “catch fireflies”. This task requires animals to actively sample from a closed-loop visual environment while concurrently computing latent variables: the evolving distance and angle to a memorized firefly. We observed mixed selectivity in all areas, with even a traditionally sensory area (MSTd) tracking latent variables. Strikingly, global encoding profiles and unit-to-unit coupling suggested a functional subnetwork between MSTd and dlPFC, and not between these are 7a, as anatomy would suggest. When sensory evidence was rendered scarce, lateral connectivity through neuron-to-neuron coupling within MSTd strengthened but its pattern remains fixed, while neuronal coupling adaptively remapped within 7a and dlPFC. The larger the remapping in 7a/dlPFC and the greater the stability within MSTd, the less was behavior impacted by loss of sensory evidence. These results highlight the distributed nature of neural coding during closed-loop action- perception naturalistic behaviors and suggest internal models may be housed in the pattern of fine-grain lateral connectivity within parietal and frontal cortices.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 24, 2021.
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Flexible neural coding in sensory, parietal, and frontal cortices during goal-directed virtual navigation
Jean-Paul Noel, Edoardo Balzani, Eric Avila, Kaushik Lakshminarasimhan, Stefania Bruni, Panos Alefantis, Cristina Savin, Dora E. Angelaki
bioRxiv 2021.10.22.465526; doi: https://doi.org/10.1101/2021.10.22.465526
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Flexible neural coding in sensory, parietal, and frontal cortices during goal-directed virtual navigation
Jean-Paul Noel, Edoardo Balzani, Eric Avila, Kaushik Lakshminarasimhan, Stefania Bruni, Panos Alefantis, Cristina Savin, Dora E. Angelaki
bioRxiv 2021.10.22.465526; doi: https://doi.org/10.1101/2021.10.22.465526

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