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 LI 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.
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).
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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- Neuroscience
Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.
