Mesoscopic-scale functional networks in the primate amygdala

  1. Jeremiah K Morrow
  2. Michael X Cohen
  3. Katalin M Gothard  Is a corresponding author
  1. University of Arizona, United States
  2. Radboud University Nijmegen, Netherlands

Abstract

The primate amygdala performs multiple functions that may be related to the anatomical heterogeneity of its nuclei. Individual neurons with stimulus- and task-specific responses are not clustered in any of the nuclei, suggesting that single-units may be too-fine grained to shed light on the mesoscale organization of the amygdala. We have extracted from local field potentials recorded simultaneously from multiple locations within the primate (Macaca mulatta) amygdala spatially defined and statistically separable responses to visual, tactile, and auditory stimuli. A generalized eigendecomposition-based method of source separation isolated coactivity patterns, or components, that in neurophysiological terms correspond to putative subnetworks. Some component spatial patterns mapped onto the anatomical organization of the amygdala, while other components reflected integration across nuclei. These components differentiated between visual, tactile, and auditory stimuli suggesting the presence of functionally distinct parallel subnetworks.

Data availability

All source data (i.e., the raw LFP from all recording sessions) have been deposited in the Zenodo repository (https://doi.org/10.5281/zenodo.3752137). The MATLAB scripts and supporting Excel data files used to process the data shown in each figure are provided with this submission.

The following data sets were generated

Article and author information

Author details

  1. Jeremiah K Morrow

    Department of Physiology, University of Arizona, Tucson, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael X Cohen

    Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1879-3593
  3. Katalin M Gothard

    Department of Physiology, University of Arizona, Tucson, United States
    For correspondence
    kgothard@email.arizona.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9642-2985

Funding

National Institute of Mental Health (P50MH100023)

  • Katalin M Gothard

National Institute of Mental Health (R01MH121009)

  • Katalin M Gothard

European Research Council (StG 638589)

  • Michael X Cohen

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

Ethics

Animal experimentation: All procedures comply with the NIH guidelines for the use of non-human primates in research as outlined in the Guide for the Care and Use of Laboratory Animals and have been approved by the Institutional Animal Care and Use Committee of the University of Arizona (protocol #08‐101).

Reviewing Editor

  1. Daeyeol Lee, Johns Hopkins University, United States

Publication history

  1. Received: March 27, 2020
  2. Accepted: August 24, 2020
  3. Accepted Manuscript published: September 2, 2020 (version 1)
  4. Version of Record published: September 14, 2020 (version 2)

Copyright

© 2020, Morrow 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

  • 1,540
    Page views
  • 165
    Downloads
  • 4
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Crossref, Scopus.

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. Jeremiah K Morrow
  2. Michael X Cohen
  3. Katalin M Gothard
(2020)
Mesoscopic-scale functional networks in the primate amygdala
eLife 9:e57341.
https://doi.org/10.7554/eLife.57341
  1. Further reading

Further reading

    1. Neuroscience
    Maria Cecilia Martinez, Camila Lidia Zold ... Mariano Andrés Belluscio
    Research Article

    The automatic initiation of actions can be highly functional. But occasionally these actions cannot be withheld and are released at inappropriate times, impulsively. Striatal activity has been shown to participate in the timing of action sequence initiation and it has been linked to impulsivity. Using a self-initiated task, we trained adult male rats to withhold a rewarded action sequence until a waiting time interval has elapsed. By analyzing neuronal activity we show that the striatal response preceding the initiation of the learned sequence is strongly modulated by the time subjects wait before eliciting the sequence. Interestingly, the modulation is steeper in adolescent rats, which show a strong prevalence of impulsive responses compared to adults. We hypothesize this anticipatory striatal activity reflects the animals’ subjective reward expectation, based on the elapsed waiting time, while the steeper waiting modulation in adolescence reflects age-related differences in temporal discounting, internal urgency states, or explore–exploit balance.

    1. Computational and Systems Biology
    2. Neuroscience
    Sergio Oscar Verduzco-Flores, Erik De Schutter
    Research Article Updated

    How dynamic interactions between nervous system regions in mammals performs online motor control remains an unsolved problem. In this paper, we show that feedback control is a simple, yet powerful way to understand the neural dynamics of sensorimotor control. We make our case using a minimal model comprising spinal cord, sensory and motor cortex, coupled by long connections that are plastic. It succeeds in learning how to perform reaching movements of a planar arm with 6 muscles in several directions from scratch. The model satisfies biological plausibility constraints, like neural implementation, transmission delays, local synaptic learning and continuous online learning. Using differential Hebbian plasticity the model can go from motor babbling to reaching arbitrary targets in less than 10 min of in silico time. Moreover, independently of the learning mechanism, properly configured feedback control has many emergent properties: neural populations in motor cortex show directional tuning and oscillatory dynamics, the spinal cord creates convergent force fields that add linearly, and movements are ataxic (as in a motor system without a cerebellum).