Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine

Brombas, Arne, Fletcher, Lee N. and Williams, Stephen R. (2014) Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine. Journal of Neuroscience, 34 5: 1932-1941. doi:10.1523/JNEUROSCI.4470-13.2014

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Author Brombas, Arne
Fletcher, Lee N.
Williams, Stephen R.
Title Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine
Journal name Journal of Neuroscience   Check publisher's open access policy
ISSN 0270-6474
Publication date 2014-01-01
Year available 2014
Sub-type Article (original research)
DOI 10.1523/JNEUROSCI.4470-13.2014
Open Access Status File (Publisher version)
Volume 34
Issue 5
Start page 1932
End page 1941
Total pages 10
Place of publication Washington, DC, United States
Publisher Society for Neuroscience
Language eng
Abstract Layer 1 neocortical GABAergic interneurons control the excitability of pyramidal neurons through cell-class-specific direct inhibitory and disynaptic disinhibitory circuitry. The engagement of layer 1 inhibitory circuits during behavior is powerfully controlled by the cholinergic neuromodulatory system. Here we report that acetylcholine (ACh) influences the excitability of layer 1 interneurons in a cell-class and activity-dependent manner. Whole-cell recordings from identified layer 1 interneurons of the rat somatosensory neocortex revealed that brief perisomatic application of ACh excited both neurogliaform cells (NGFCs) and classical-accommodating cells (c-ACs) at rest by the activation of nicotinic receptors. In contrast, under active, action potential firing states, ACh excited c-ACs, but inhibited NGFCs through muscarinic receptor-mediated, IP3 receptor-dependent elevations of intracellular calcium that gated surface-membrane calcium-activated potassium channels. These excitatory and inhibitory actions of ACh could be switched between by brief periods of NGFC action potential firing. Paired recordings demonstrated that cholinergic inhibition of NGFCs disinhibited the apical dendrites of layer 2/3 pyramidal neurons by silencing widespread, GABAB receptor-mediated, monosynaptic inhibition. Together, these data suggest that the cholinergic system modulates layer 1 inhibitory circuits in an activity-dependent manner to dynamically control dendritic synaptic inhibition of pyramidal neurons.
Keyword Axon
Synaptic integration
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Queensland Brain Institute Publications
Official 2015 Collection
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