Gamma rhythms and visual information in mouse V1 specifically modulated by somatostatin+ neurons in reticular thalamus

  1. Mahmood S Hoseini
  2. Bryan Higashikubo
  3. Frances S Cho
  4. Andrew H Chang
  5. Alexandra Clemente-Perez
  6. Irene Lew
  7. Agnieszka Ciesielska
  8. Michael P Stryker
  9. Jeanne T Paz  Is a corresponding author
  1. University of California, San Francisco, United States
  2. Gladstone Institutes, United States

Abstract

Visual perception in natural environments depends on the ability to focus on salient stimuli while ignoring distractions. This kind of selective visual attention is associated with gamma activity in the visual cortex. While the nucleus reticularis thalami (nRT) has been implicated in selective attention, its role in modulating gamma activity in the visual cortex remains unknown. Here we show that somatostatin- (SST) but not parvalbumin-expressing (PV) neurons in the visual sector of the nRT preferentially project to the dorsal lateral geniculate nucleus (dLGN), and modulate visual information transmission and gamma activity in primary visual cortex (V1). These findings pinpoint the SST neurons in nRT as powerful modulators of the visual information encoding accuracy in V1, and represent a novel circuit through which the nRT can influence representation of visual information.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data for all figures are available in a spreadsheet format.

Article and author information

Author details

  1. Mahmood S Hoseini

    Department of Physiology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3139-0561
  2. Bryan Higashikubo

    Neurology, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Frances S Cho

    Neurology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrew H Chang

    Neurology, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexandra Clemente-Perez

    Neuroscience Graduate Program, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Irene Lew

    Neurology, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Agnieszka Ciesielska

    Neurology, Gladstone Institutes, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Michael P Stryker

    Center for Integrative Neuroscience, Department of Physiology, University of California, San Francisco, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Jeanne T Paz

    Neurology, Gladstone Institutes, San Francisco, United States
    For correspondence
    jeanne.paz@gladstone.ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6339-8130

Funding

National Institute of Neurological Disorders and Stroke (NS096369)

  • Jeanne T Paz

National Science Foundation (1822598)

  • Michael P Stryker

National Institute for Health Research (EY025174)

  • Michael P Stryker

American Epilepsy Society

  • Bryan Higashikubo

National Institute of Neurological Disorders and Stroke (F31NA111819)

  • Frances S Cho

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

Reviewing Editor

  1. Solange P Brown, Johns Hopkins University, United States

Ethics

Animal experimentation: We performed all experiments in compliance with protocols approved by the Institutional Animal Care and Use Committees at the University of California, San Francisco and Gladstone Institutes (protocol numbers AN180588-02C and AN174396-03E). Precautions were taken to minimize stress and the number of animals used in all experiments. We followed the NIH guidelines for rigor and reproducibility of the research.

Version history

  1. Received: July 25, 2020
  2. Accepted: April 11, 2021
  3. Accepted Manuscript published: April 12, 2021 (version 1)
  4. Version of Record published: April 23, 2021 (version 2)

Copyright

© 2021, Hoseini 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

  • 2,752
    Page views
  • 387
    Downloads
  • 6
    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. Mahmood S Hoseini
  2. Bryan Higashikubo
  3. Frances S Cho
  4. Andrew H Chang
  5. Alexandra Clemente-Perez
  6. Irene Lew
  7. Agnieszka Ciesielska
  8. Michael P Stryker
  9. Jeanne T Paz
(2021)
Gamma rhythms and visual information in mouse V1 specifically modulated by somatostatin+ neurons in reticular thalamus
eLife 10:e61437.
https://doi.org/10.7554/eLife.61437

Share this article

https://doi.org/10.7554/eLife.61437

Further reading

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Medicine
    2. Neuroscience
    Luisa Fassi, Shachar Hochman ... Roi Cohen Kadosh
    Research Article

    In recent years, there has been debate about the effectiveness of treatments from different fields, such as neurostimulation, neurofeedback, brain training, and pharmacotherapy. This debate has been fuelled by contradictory and nuanced experimental findings. Notably, the effectiveness of a given treatment is commonly evaluated by comparing the effect of the active treatment versus the placebo on human health and/or behaviour. However, this approach neglects the individual’s subjective experience of the type of treatment she or he received in establishing treatment efficacy. Here, we show that individual differences in subjective treatment - the thought of receiving the active or placebo condition during an experiment - can explain variability in outcomes better than the actual treatment. We analysed four independent datasets (N = 387 participants), including clinical patients and healthy adults from different age groups who were exposed to different neurostimulation treatments (transcranial magnetic stimulation: Studies 1 and 2; transcranial direct current stimulation: Studies 3 and 4). Our findings show that the inclusion of subjective treatment can provide a better model fit either alone or in interaction with objective treatment (defined as the condition to which participants are assigned in the experiment). These results demonstrate the significant contribution of subjective experience in explaining the variability of clinical, cognitive, and behavioural outcomes. We advocate for existing and future studies in clinical and non-clinical research to start accounting for participants’ subjective beliefs and their interplay with objective treatment when assessing the efficacy of treatments. This approach will be crucial in providing a more accurate estimation of the treatment effect and its source, allowing the development of effective and reproducible interventions.