Thalamic reticular nucleus induces fast and local modulation of arousal state

  1. Laura D Lewis
  2. Jakob Voigts
  3. Francisco J Flores
  4. Lukas I Schmitt
  5. Matthew A Wilson
  6. Michael M Halassa
  7. Emery N Brown  Is a corresponding author
  1. Harvard University, United States
  2. Massachusetts Institute of Technology, United States
  3. New York University, United States

Abstract

During low arousal states such as drowsiness and sleep, cortical neurons exhibit rhythmic slow wave activity associated with periods of neuronal silence. Slow waves are locally regulated, and local slow wave dynamics are important for memory, cognition, and behaviour. While several brainstem structures for controlling global sleep states have now been well characterized, a mechanism underlying fast and local modulation of cortical slow waves has not been identified. Here, using optogenetics and whole cortex electrophysiology, we show that local tonic activation of thalamic reticular nucleus (TRN) rapidly induces slow wave activity in a spatially restricted region of cortex. These slow waves resemble those seen in sleep, as cortical units undergo periods of silence phase-locked to the slow wave. Furthermore, animals exhibit behavioural changes consistent with a decrease in arousal state during TRN stimulation. We conclude that TRN can induce rapid modulation of local cortical state.

Article and author information

Author details

  1. Laura D Lewis

    Society of Fellows, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  2. Jakob Voigts

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
  3. Francisco J Flores

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
  4. Lukas I Schmitt

    Neuroscience Institute, New York University, New York, United States
    Competing interests
    No competing interests declared.
  5. Matthew A Wilson

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    No competing interests declared.
  6. Michael M Halassa

    Neuroscience Institute, New York University, New York, United States
    Competing interests
    No competing interests declared.
  7. Emery N Brown

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    enb@neurostat.mit.edu
    Competing interests
    Emery N Brown, Reviewing editor, eLife.

Ethics

Animal experimentation: All experimental procedures were approved by the MIT Committee on Animal Care (protocol number #0514-038-17).

Copyright

© 2015, Lewis 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

  • 8,562
    views
  • 2,254
    downloads
  • 150
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Laura D Lewis
  2. Jakob Voigts
  3. Francisco J Flores
  4. Lukas I Schmitt
  5. Matthew A Wilson
  6. Michael M Halassa
  7. Emery N Brown
(2015)
Thalamic reticular nucleus induces fast and local modulation of arousal state
eLife 4:e08760.
https://doi.org/10.7554/eLife.08760

Share this article

https://doi.org/10.7554/eLife.08760

Further reading

    1. Neuroscience
    Xinlin Hou, Peng Zhang ... Dandan Zhang
    Research Article

    Emotional responsiveness in neonates, particularly their ability to discern vocal emotions, plays an evolutionarily adaptive role in human communication and adaptive behaviors. The developmental trajectory of emotional sensitivity in neonates is crucial for understanding the foundations of early social-emotional functioning. However, the precise onset of this sensitivity and its relationship with gestational age (GA) remain subjects of investigation. In a study involving 120 healthy neonates categorized into six groups based on their GA (ranging from 35 and 40 weeks), we explored their emotional responses to vocal stimuli. These stimuli encompassed disyllables with happy and neutral prosodies, alongside acoustically matched nonvocal control sounds. The assessments occurred during natural sleep states using the odd-ball paradigm and event-related potentials. The results reveal a distinct developmental change at 37 weeks GA, marking the point at which neonates exhibit heightened perceptual acuity for emotional vocal expressions. This newfound ability is substantiated by the presence of the mismatch response, akin to an initial form of adult mismatch negativity, elicited in response to positive emotional vocal prosody. Notably, this perceptual shift’s specificity becomes evident when no such discrimination is observed in acoustically matched control sounds. Neonates born before 37 weeks GA do not display this level of discrimination ability. This developmental change has important implications for our understanding of early social-emotional development, highlighting the role of gestational age in shaping early perceptual abilities. Moreover, while these findings introduce the potential for a valuable screening tool for conditions like autism, characterized by atypical social-emotional functions, it is important to note that the current data are not yet robust enough to fully support this application. This study makes a substantial contribution to the broader field of developmental neuroscience and holds promise for future research on early intervention in neurodevelopmental disorders.

    1. Neuroscience
    Luis Alberto Bezares Calderón, Réza Shahidi, Gáspár Jékely
    Research Article

    Hydrostatic pressure is a dominant environmental cue for vertically migrating marine organisms but the physiological mechanisms of responding to pressure changes remain unclear. Here, we uncovered the cellular and circuit bases of a barokinetic response in the planktonic larva of the marine annelid Platynereis dumerilii. Increased pressure induced a rapid, graded, and adapting upward swimming response due to the faster beating of cilia in the head multiciliary band. By calcium imaging, we found that brain ciliary photoreceptors showed a graded response to pressure changes. The photoreceptors in animals mutant for ciliary opsin-1 had a smaller sensory compartment and mutant larvae showed diminished pressure responses. The ciliary photoreceptors synaptically connect to the head multiciliary band via serotonergic motoneurons. Genetic inhibition of the serotonergic cells blocked pressure-dependent increases in ciliary beating. We conclude that ciliary photoreceptors function as pressure sensors and activate ciliary beating through serotonergic signalling during barokinesis.