Ultrafast (400 Hz) network oscillations induced in mouse barrel cortex by optogenetic activation of thalamocortical axons

  1. Hang Hu
  2. Rachel E Hostetler
  3. Ariel Agmon  Is a corresponding author
  1. West Virginia University, United States

Abstract

Oscillations of extracellular voltage, reflecting synchronous, rhythmic activity in large populations of neurons, are a ubiquitous feature in the mammalian brain and are thought to subserve important, if not fully understood cognitive functions. Oscillations at different frequency bands are hallmarks of specific brain and behavioral states. At the higher end of the spectrum, ultrafast (400-600 Hz) oscillations in the somatosensory cortex, in response to peripheral nerve stimulation or punctate sensory stimuli, were previously observed in humans and in a handful of animal studies; however, their synaptic basis and functional significance remain largely unexplored. Here we report that brief optogenetic activation of thalamocortical axons, in brain slices from mouse somatosensory (barrel) cortex, elicited in the thalamorecipient layer local field potential (LFP) oscillations which we dubbed 'ripplets', consisting of a sequence of precisely reproducible 2-5 negative transients at ~400 Hz which originated in the postsynaptic cortical network. Fast-spiking (FS) inhibitory interneurons fired ~400 Hz spike bursts entrained to the LFP oscillation, while regular-spiking (RS) excitatory neurons typically fired only 1-2 spikes per ripplet, preceding FS spikes by ~1.5 ms. Spike bursts were exquisitely synchronized between neighboring FS cells, while RS cells received synchronous, precisely repeating sequences of alternating excitatory and inhibitory postsynaptic currents (E/IPSCs) phase-locked to the LFP oscillation. Spikes in FS cells followed at short (~0.4 ms) latency onset of EPSCs and preceded (by ~0.8 ms) onset of IPSCs in simultaneously recorded RS cells, suggesting that FS cells were driven to fire by phasic inputs from excitatory cells, and in turn evoked volleys of inhibition which enforced synchrony on excitatory cells. We suggest that ripplets are an intrinsically generated cortical response to a strong, synchronous thalamocortical volley. Ripplets and the associated spike sequences in excitatory cells could provide increased bandwidth for encoding and transmitting sensory information. In addition, optogenetically induced ripplets are a uniquely accessible model system for studying synaptic mechanisms of fast and ultrafast cortical and hippocampal oscillations.

Data availability

Figure 1- Source Data 1 contains the cell count data used for Figure 1 - Figure Supplement 1;Figure 2- Source Data 1 contains the electrophysiological parameters data used for Figure 2 - Figure Supplement 1;Code used to calculate synchrony indices has been deposited to GitHub.

Article and author information

Author details

  1. Hang Hu

    Department of Neuroscience, West Virginia University, Morgantown, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Rachel E Hostetler

    Department of Neuroscience, West Virginia University, Morgantown, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4185-6468
  3. Ariel Agmon

    Department of Neuroscience, West Virginia University, Morgantown, United States
    For correspondence
    aric.agmon@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7556-8130

Funding

National Institutes of Health (NS116604)

  • Ariel Agmon

National Institutes of Health (Predoctoral Training Grants GM081741 and GM132494)

  • Rachel E Hostetler

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

Ethics

Animal experimentation: Animals used in this study were housed at the AAALAC-accredited WVU Lab Animal Research Facility according to institutional, federal and AAALAC guidelines. Animal use followed the Public Health Service Policy on Humane Care and Use of Laboratory Animals, and was approved by the WVU Institutional Animal Care and Use Committee (protocol #1604002316). West Virginia University has a PHS-approved Animal Welfare Assurance D16-00362 (A3597-01).

Reviewing Editor

  1. Eunji Cheong, Yonsei University, Republic of Korea

Publication history

  1. Received: August 3, 2022
  2. Preprint posted: September 5, 2022 (view preprint)
  3. Accepted: April 28, 2023
  4. Accepted Manuscript published: May 9, 2023 (version 1)
  5. Version of Record published: May 25, 2023 (version 2)

Copyright

© 2023, Hu 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

  • 443
    Page views
  • 65
    Downloads
  • 0
    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. Hang Hu
  2. Rachel E Hostetler
  3. Ariel Agmon
(2023)
Ultrafast (400 Hz) network oscillations induced in mouse barrel cortex by optogenetic activation of thalamocortical axons
eLife 12:e82412.
https://doi.org/10.7554/eLife.82412

Further reading

    1. Neuroscience
    Xiaosha Wang, Bijun Wang, Yanchao Bi
    Research Article Updated

    One signature of the human brain is its ability to derive knowledge from language inputs, in addition to nonlinguistic sensory channels such as vision and touch. How does human language experience modulate the mechanism by which semantic knowledge is stored in the human brain? We investigated this question using a unique human model with varying amounts and qualities of early language exposure: early deaf adults who were born to hearing parents and had reduced early exposure and delayed acquisition of any natural human language (speech or sign), with early deaf adults who acquired sign language from birth as the control group that matches on nonlinguistic sensory experiences. Neural responses in a semantic judgment task with 90 written words that were familiar to both groups were measured using fMRI. The deaf group with reduced early language exposure, compared with the deaf control group, showed reduced semantic sensitivity, in both multivariate pattern (semantic structure encoding) and univariate (abstractness effect) analyses, in the left dorsal anterior temporal lobe (dATL). These results provide positive, causal evidence that language experience drives the neural semantic representation in the dATL, highlighting the roles of language in forming human neural semantic structures beyond nonverbal sensory experiences.

    1. Neuroscience
    Ayako Yamaguchi, Manon Peltier
    Research Article Updated

    Across phyla, males often produce species-specific vocalizations to attract females. Although understanding the neural mechanisms underlying behavior has been challenging in vertebrates, we previously identified two anatomically distinct central pattern generators (CPGs) that drive the fast and slow clicks of male Xenopus laevis, using an ex vivo preparation that produces fictive vocalizations. Here, we extended this approach to four additional species, X. amieti, X. cliivi, X. petersii, and X. tropicalis, by developing ex vivo brain preparation from which fictive vocalizations are elicited in response to a chemical or electrical stimulus. We found that even though the courtship calls are species-specific, the CPGs used to generate clicks are conserved across species. The fast CPGs, which critically rely on reciprocal connections between the parabrachial nucleus and the nucleus ambiguus, are conserved among fast-click species, and slow CPGs are shared among slow-click species. In addition, our results suggest that testosterone plays a role in organizing fast CPGs in fast-click species, but not in slow-click species. Moreover, fast CPGs are not inherited by all species but monopolized by fast-click species. The results suggest that species-specific calls of the genus Xenopus have evolved by utilizing conserved slow and/or fast CPGs inherited by each species.