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.

Reviewing Editor

  1. Daeyeol Lee, Johns Hopkins University, United States

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).

Version 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

  • 1,684
    Page views
  • 191
    Downloads
  • 4
    Citations

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

Share this article

https://doi.org/10.7554/eLife.57341

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.