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
Brain states fluctuate between exploratory and consummatory phases of behavior. These state changes affect both internal computation and the organism’s responses to sensory inputs. Understanding neuronal mechanisms supporting exploratory and consummatory states and their switching requires experimental control of behavioral shifts and collecting sufficient amounts of brain data. To achieve this goal, we developed the ThermoMaze, which exploits the animal’s natural warmth-seeking homeostatic behavior. By decreasing the floor temperature and selectively heating unmarked areas, we observed that mice avoided the aversive state by exploring the maze and finding the warm spot. In its design, the ThermoMaze is analogous to the widely used water maze but without the inconvenience of a wet environment and, therefore, allows the collection of physiological data in many trials. We combined the ThermoMaze with electrophysiology recording, and report that spiking activity of hippocampal CA1 neurons during sharp-wave ripple events encode the position of mice. Thus, place-specific firing is not confined to locomotion and associated theta oscillations but persist during waking immobility and sleep at the same location. The ThermoMaze will allow for detailed studies of brain correlates of immobility, preparatory–consummatory transitions, and open new options for studying behavior-mediated temperature homeostasis.
