Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex
- University of Edinburgh, United Kingdom
Abstract
Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.
Article and author information
Author details
Nathalie L Rochefort
Funding
Wellcome (102857/Z/13/Z)
- Nathalie LI Rochefort
EuroSpin Erasmus Mundus Program
- Sander W Keemink
Royal Society (102857/Z/13/Z)
- Nathalie LI Rochefort
European Commission (Marie Curie Actions (FP7), MC-CIG 631770)
- Nathalie LI Rochefort
Patrick Wild Centre
- Nathalie LI Rochefort
The Shirley Foundation
- Nathalie LI Rochefort
RS MacDonald Charitable Trust (Seedcorn Grant 21)
- Nathalie LI Rochefort
University Of Edinburgh (Graduate School of Life Sciences)
- Evelyn Dylda
European Commission (Marie Curie Actions (FP7), IEF 624461)
- Janelle MP Pakan
EPSRC Doctoral Training Centre in Neuroinformatics (EP/F500385/1 and BB/F529254/1)
- Sander W Keemink
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Thomas D Mrsic-Flogel, University of Basel, Switzerland
Ethics
Animal experimentation: All procedures were approved by the University of Edinburgh animal welfare committee, and were performed under a UK Home Office Project License (PPL No. 60/4570).
Version history
- Received: February 3, 2016
- Accepted: August 22, 2016
- Accepted Manuscript published: August 23, 2016 (version 1)
- Accepted Manuscript updated: September 2, 2016 (version 2)
- Accepted Manuscript updated: September 9, 2016 (version 3)
- Version of Record published: September 20, 2016 (version 4)
- Version of Record updated: September 6, 2017 (version 5)
Copyright
© 2016, Pakan 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.
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Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex
eLife 5:e14985.
https://doi.org/10.7554/eLife.14985
Further reading
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- Biochemistry and Chemical Biology
- Neuroscience
In most mammals, conspecific chemosensory communication relies on semiochemical release within complex bodily secretions and subsequent stimulus detection by the vomeronasal organ (VNO). Urine, a rich source of ethologically relevant chemosignals, conveys detailed information about sex, social hierarchy, health, and reproductive state, which becomes accessible to a conspecific via vomeronasal sampling. So far, however, numerous aspects of social chemosignaling along the vomeronasal pathway remain unclear. Moreover, since virtually all research on vomeronasal physiology is based on secretions derived from inbred laboratory mice, it remains uncertain whether such stimuli provide a true representation of potentially more relevant cues found in the wild. Here, we combine a robust low-noise VNO activity assay with comparative molecular profiling of sex- and strain-specific mouse urine samples from two inbred laboratory strains as well as from wild mice. With comprehensive molecular portraits of these secretions, VNO activity analysis now enables us to (i) assess whether and, if so, how much sex/strain-selective ‘raw’ chemical information in urine is accessible via vomeronasal sampling; (ii) identify which chemicals exhibit sufficient discriminatory power to signal an animal’s sex, strain, or both; (iii) determine the extent to which wild mouse secretions are unique; and (iv) analyze whether vomeronasal response profiles differ between strains. We report both sex- and, in particular, strain-selective VNO representations of chemical information. Within the urinary ‘secretome’, both volatile compounds and proteins exhibit sufficient discriminative power to provide sex- and strain-specific molecular fingerprints. While total protein amount is substantially enriched in male urine, females secrete a larger variety at overall comparatively low concentrations. Surprisingly, the molecular spectrum of wild mouse urine does not dramatically exceed that of inbred strains. Finally, vomeronasal response profiles differ between C57BL/6 and BALB/c animals, with particularly disparate representations of female semiochemicals.
