1. Neuroscience
Download icon

Variation of connectivity across exemplar sensory and associative thalamocortical loops in the mouse

  1. Arghya Mukherjee  Is a corresponding author
  2. Navdeep Bajwa
  3. Norman H Lam
  4. César Porrero
  5. Francisco Clasca
  6. Michael M Halassa  Is a corresponding author
  1. Massachusetts Institute of Technology, United States
  2. Autonoma University of Madrid, Spain
Research Article
  • Cited 1
  • Views 2,615
  • Annotations
Cite this article as: eLife 2020;9:e62554 doi: 10.7554/eLife.62554

Abstract

The thalamus engages in sensation, action, and cognition, but the structure underlying these functions is poorly understood. Thalamic innervation of associative cortex targets several interneuron types, modulating dynamics and influencing plasticity. Is this structure-function relationship distinct from that of sensory thalamocortical systems? Here, we systematically compared function and structure across a sensory and an associative thalamocortical loop in the mouse. Enhancing excitability of mediodorsal thalamus, an associative structure, resulted in prefrontal activity dominated by inhibition. Equivalent enhancement of medial geniculate excitability robustly drove auditory cortical excitation. Structurally, geniculate axons innervated excitatory cortical targets in a preferential manner and with larger synaptic terminals, providing a putative explanation for functional divergence. The two thalamic circuits also had distinct input patterns, with mediodorsal thalamus receiving innervation from a diverse set of cortical areas. Altogether, our findings contribute to the emerging view of functional diversity across thalamic microcircuits and its structural basis.

Data availability

All data generated or analyzed are included in the manuscript as source data files for Figures 1 to 7.

Article and author information

Author details

  1. Arghya Mukherjee

    Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    mukhargh@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3341-4408
  2. Navdeep Bajwa

    Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Norman H Lam

    Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. César Porrero

    Anatomy and Neuroscience, Autonoma University of Madrid, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Francisco Clasca

    Anatomy and Neuroscience, Autonoma University of Madrid, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0718-1337
  6. Michael M Halassa

    Neuroscience Institute, Massachusetts Institute of Technology, New York, United States
    For correspondence
    mhalassa@mit.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Commission (945539-HBP-SGA3)

  • Francisco Clasca

National Institute of Mental Health (R01MH120118)

  • Michael M Halassa

National Institute of Mental Health (R01MH107680)

  • Michael M Halassa

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 animal experiments were performed according to the guidelines of the US National Institutes of Health and the Institutional Animal Care and Use Committee at the Massachusetts Institute of Technology. Experimental procedures for bouton analysis as shown in figure 4 were approved by the Autonoma de Madrid University ethics committee and the corresponding Madrid Regional Government agency (PROEX175/16), in accordance with the European Community Council Directive 2010/63/UE.

Reviewing Editor

  1. Mathieu Wolff, CNRS, University of Bordeaux, France

Publication history

  1. Received: August 28, 2020
  2. Accepted: October 23, 2020
  3. Accepted Manuscript published: October 26, 2020 (version 1)
  4. Version of Record published: November 5, 2020 (version 2)

Copyright

© 2020, Mukherjee 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

  • 2,615
    Page views
  • 339
    Downloads
  • 1
    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)

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

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

Further reading

    1. Neuroscience
    Debora Fusca, Peter Kloppenburg
    Research Article

    Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

    1. Neuroscience
    Wanhui Sheng et al.
    Research Article Updated

    Hypothalamic oxytocinergic magnocellular neurons have a fascinating ability to release peptide from both their axon terminals and from their dendrites. Existing data indicates that the relationship between somatic activity and dendritic release is not constant, but the mechanisms through which this relationship can be modulated are not completely understood. Here, we use a combination of electrical and optical recording techniques to quantify activity-induced calcium influx in proximal vs. distal dendrites of oxytocinergic magnocellular neurons located in the paraventricular nucleus of the hypothalamus (OT-MCNs). Results reveal that the dendrites of OT-MCNs are weak conductors of somatic voltage changes; however, activity-induced dendritic calcium influx can be robustly regulated by both osmosensitive and non-osmosensitive ion channels located along the dendritic membrane. Overall, this study reveals that dendritic conductivity is a dynamic and endogenously regulated feature of OT-MCNs that is likely to have substantial functional impact on central oxytocin release.