Functional links between sensory representations, choice activity, and sensorimotor associations in parietal cortex

  1. Ting-Yu Chang
  2. Raymond Doudlah
  3. Byounghoon Kim
  4. Adhira Sunkara
  5. Lowell W Thompson
  6. Meghan E Lowe
  7. Ari Rosenberg  Is a corresponding author
  1. University of Wisconsin - Madison, United States
  2. WiSys Technology Foundation, United States

Abstract

Three-dimensional (3D) representations of the environment are often critical for selecting actions that achieve desired goals. The success of these goal-directed actions relies on 3D sensorimotor transformations that are experience-dependent. Here we investigated the relationships between the robustness of 3D visual representations, choice-related activity, and motor-related activity in parietal cortex. Macaque monkeys performed an eight-alternative 3D orientation discrimination task and a visually guided saccade task while we recorded from the caudal intraparietal area using laminar probes. We found that neurons with more robust 3D visual representations preferentially carried choice-related activity. Following the onset of choice-related activity, the robustness of the 3D representations further increased for those neurons. We additionally found that 3D orientation and saccade direction preferences aligned, particularly for neurons with choice-related activity, reflecting an experience-dependent sensorimotor association. These findings reveal previously unrecognized links between the fidelity of ecologically relevant object representations, choice-related activity, and motor-related activity.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Ting-Yu Chang

    Neuroscience, University of Wisconsin - Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3964-0905
  2. Raymond Doudlah

    Neuroscience, University of Wisconsin - Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Byounghoon Kim

    Neuroscience, University of Wisconsin - Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7159-5134
  4. Adhira Sunkara

    WiSys Technology Foundation, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Lowell W Thompson

    Neuroscience, University of Wisconsin - Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Meghan E Lowe

    Neuroscience, University of Wisconsin - Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ari Rosenberg

    Neuroscience, University of Wisconsin - Madison, Madison, United States
    For correspondence
    ari.rosenberg@wisc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8606-2987

Funding

Alfred P. Sloan Foundation (FG-2016-6468)

  • Ari Rosenberg

Whitehall Foundation (2016-08-18)

  • Ari Rosenberg

Greater Milwaukee Foundation (Shaw Scientist Award)

  • Ari Rosenberg

National Institutes of Health (EY029438)

  • Ari Rosenberg

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David J Freedman, The University of Chicago, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations of the National Institutes of Health's Guide for the Care and Use of Laboratory Animals. All experimental procedures and surgeries were approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Wisconsin-Madison (Protocol #: G005229).

Version history

  1. Received: April 16, 2020
  2. Accepted: October 19, 2020
  3. Accepted Manuscript published: October 20, 2020 (version 1)
  4. Version of Record published: November 4, 2020 (version 2)

Copyright

© 2020, Chang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,396
    views
  • 180
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Ting-Yu Chang
  2. Raymond Doudlah
  3. Byounghoon Kim
  4. Adhira Sunkara
  5. Lowell W Thompson
  6. Meghan E Lowe
  7. Ari Rosenberg
(2020)
Functional links between sensory representations, choice activity, and sensorimotor associations in parietal cortex
eLife 9:e57968.
https://doi.org/10.7554/eLife.57968

Share this article

https://doi.org/10.7554/eLife.57968

Further reading

    1. Neuroscience
    Alyssa D Huff, Marlusa Karlen-Amarante ... Jan-Marino Ramirez
    Research Advance

    Obstructive sleep apnea (OSA) is a prevalent sleep-related breathing disorder that results in multiple bouts of intermittent hypoxia. OSA has many neurological and systemic comorbidities, including dysphagia, or disordered swallow, and discoordination with breathing. However, the mechanism in which chronic intermittent hypoxia (CIH) causes dysphagia is unknown. Recently, we showed the postinspiratory complex (PiCo) acts as an interface between the swallow pattern generator (SPG) and the inspiratory rhythm generator, the preBötzinger complex, to regulate proper swallow-breathing coordination (Huff et al., 2023). PiCo is characterized by interneurons co-expressing transporters for glutamate (Vglut2) and acetylcholine (ChAT). Here we show that optogenetic stimulation of ChATcre:Ai32, Vglut2cre:Ai32, and ChATcre:Vglut2FlpO:ChR2 mice exposed to CIH does not alter swallow-breathing coordination, but unexpectedly disrupts swallow behavior via triggering variable swallow motor patterns. This suggests that glutamatergic–cholinergic neurons in PiCo are not only critical for the regulation of swallow-breathing coordination, but also play an important role in the modulation of swallow motor patterning. Our study also suggests that swallow disruption, as seen in OSA, involves central nervous mechanisms interfering with swallow motor patterning and laryngeal activation. These findings are crucial for understanding the mechanisms underlying dysphagia, both in OSA and other breathing and neurological disorders.

    1. Neuroscience
    Vezha Boboeva, Alberto Pezzotta ... Athena Akrami
    Research Article

    The central tendency bias, or contraction bias, is a phenomenon where the judgment of the magnitude of items held in working memory appears to be biased toward the average of past observations. It is assumed to be an optimal strategy by the brain and commonly thought of as an expression of the brain’s ability to learn the statistical structure of sensory input. On the other hand, recency biases such as serial dependence are also commonly observed and are thought to reflect the content of working memory. Recent results from an auditory delayed comparison task in rats suggest that both biases may be more related than previously thought: when the posterior parietal cortex (PPC) was silenced, both short-term and contraction biases were reduced. By proposing a model of the circuit that may be involved in generating the behavior, we show that a volatile working memory content susceptible to shifting to the past sensory experience – producing short-term sensory history biases – naturally leads to contraction bias. The errors, occurring at the level of individual trials, are sampled from the full distribution of the stimuli and are not due to a gradual shift of the memory toward the sensory distribution’s mean. Our results are consistent with a broad set of behavioral findings and provide predictions of performance across different stimulus distributions and timings, delay intervals, as well as neuronal dynamics in putative working memory areas. Finally, we validate our model by performing a set of human psychophysics experiments of an auditory parametric working memory task.