Mechanisms and functions of respiration-driven gamma oscillations in the primary olfactory cortex
Gamma oscillations are believed to underlie cognitive processes by shaping the formation of transient neuronal partnerships on a millisecond scale. These oscillations are coupled to the phase of breathing cycles in several brain areas, possibly reflecting local computations driven by sensory inputs sampled at each breath. Here, we investigated the mechanisms and functions of gamma oscillations in the piriform (olfactory) cortex of awake mice to understand their dependence on breathing and how they relate to local spiking activity. Mechanistically, we find that respiration drives gamma oscillations in the piriform cortex, which correlate with local feedback inhibition and result from recurrent connections between local excitatory and inhibitory neuronal populations. Moreover, respiration-driven gamma oscillations are triggered by the activation of mitral/tufted cells in the olfactory bulb and are abolished during ketamine/xylazine anesthesia. Functionally, we demonstrate that they locally segregate neuronal assemblies through a winner-take-all computation leading to sparse odor coding during each breathing cycle. Our results shed new light on the mechanisms of gamma oscillations, bridging computation, cognition and physiology.
All the data employed is freely available at: http://crcns.org, pcx-1 dataset. http://dx.doi.org/10.6080/K00C4SZB
Article and author information
Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Adriano BL Tort
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Adriano BL Tort
Comisión Sectorial de Investigación Científica
- Joaquin Gonzalez
- Pablo Torterolo
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Animal experimentation: The present study used a third-party dataset and required no ethical permit for the performed computational analyses. The experimental protocols of the original data source (Bolding and Franks, 2018) were approved by Duke University Institutional Animal Care and Use Committee (protocol A220-15-08).
- Laura L Colgin, University of Texas at Austin, United States
- Received: August 28, 2022
- Accepted: February 17, 2023
- Accepted Manuscript published: February 20, 2023 (version 1)
© 2023, Gonzalez 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.
- Page views
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
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)
Pattern separation, or the process by which highly similar stimuli or experiences in memory are represented by non-overlapping neural ensembles, has typically been ascribed to processes supported by the hippocampus. Converging evidence from a wide range of studies, however, suggests that pattern separation is a multistage process supported by a network of brain regions. Based on this evidence, considered together with related findings from the interference resolution literature, we propose the ‘cortico-hippocampal pattern separation’ (CHiPS) framework, which asserts that brain regions involved in cognitive control play a significant role in pattern separation. Particularly, these regions may contribute to pattern separation by (1) resolving interference in sensory regions that project to the hippocampus, thus regulating its cortical input, or (2) directly modulating hippocampal processes in accordance with task demands. Considering recent interest in how hippocampal operations are modulated by goal states likely represented and regulated by extra-hippocampal regions, we argue that pattern separation is similarly supported by neocortical–hippocampal interactions.
Chronic, or persistent pain affects more than 10% of adults in the general population. This makes it one of the major physical and mental health care problems. Although pain is an important acute warning signal that allows the organism to take action before tissue damage occurs, it can become persistent and its role as a warning signal thereby inadequate. Although per definition, pain can only be labeled as persistent after 3 months, the trajectory from acute to persistent pain is likely to be determined very early and might even start at the time of injury. The biopsychosocial model has revolutionized our understanding of chronic pain and paved the way for psychological treatments for persistent pain, which routinely outperform other forms of treatment. This suggests that psychological processes could also be important in shaping the very early trajectory from acute to persistent pain and that targeting these processes could prevent the development of persistent pain. In this review, we develop an integrative model and suggest novel interventions during early pain trajectories, based on predictions from this model.