Publication Date:
2013-10-08
Description:
In the mammalian cerebral cortex the diversity of interneuronal subtypes underlies a division of labour subserving distinct modes of inhibitory control. A unique mode of inhibitory control may be provided by inhibitory neurons that specifically suppress the firing of other inhibitory neurons. Such disinhibition could lead to the selective amplification of local processing and serve the important computational functions of gating and gain modulation. Although several interneuron populations are known to target other interneurons to varying degrees, little is known about interneurons specializing in disinhibition and their in vivo function. Here we show that a class of interneurons that express vasoactive intestinal polypeptide (VIP) mediates disinhibitory control in multiple areas of neocortex and is recruited by reinforcement signals. By combining optogenetic activation with single-cell recordings, we examined the functional role of VIP interneurons in awake mice, and investigated the underlying circuit mechanisms in vitro in auditory and medial prefrontal cortices. We identified a basic disinhibitory circuit module in which activation of VIP interneurons transiently suppresses primarily somatostatin- and a fraction of parvalbumin-expressing inhibitory interneurons that specialize in the control of the input and output of principal cells, respectively. During the performance of an auditory discrimination task, reinforcement signals (reward and punishment) strongly and uniformly activated VIP neurons in auditory cortex, and in turn VIP recruitment increased the gain of a functional subpopulation of principal neurons. These results reveal a specific cell type and microcircuit underlying disinhibitory control in cortex and demonstrate that it is activated under specific behavioural conditions.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4017628/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4017628/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Pi, Hyun-Jae -- Hangya, Balazs -- Kvitsiani, Duda -- Sanders, Joshua I -- Huang, Z Josh -- Kepecs, Adam -- R01 NS075531/NS/NINDS NIH HHS/ -- R01NS075531/NS/NINDS NIH HHS/ -- U01 MH078844/MH/NIMH NIH HHS/ -- U01MH078844/MH/NIMH NIH HHS/ -- England -- Nature. 2013 Nov 28;503(7477):521-4. doi: 10.1038/nature12676. Epub 2013 Oct 6.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, New York 11724, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/24097352" target="_blank"〉PubMed〈/a〉
Keywords:
Acoustic Stimulation
;
Animals
;
Auditory Cortex/physiology
;
Cerebral Cortex/*cytology/*physiology
;
Discrimination (Psychology)/physiology
;
Female
;
Interneurons/*physiology
;
Male
;
Mice
;
Mice, Inbred C57BL
;
Neural Inhibition/*physiology
;
Optogenetics
;
Parvalbumins/metabolism
;
Prefrontal Cortex/physiology
;
Punishment
;
Reward
;
Single-Cell Analysis
;
Somatostatin/metabolism
;
Vasoactive Intestinal Peptide/metabolism
;
Wakefulness/physiology
Print ISSN:
0028-0836
Electronic ISSN:
1476-4687
Topics:
Biology
,
Chemistry and Pharmacology
,
Medicine
,
Natural Sciences in General
,
Physics
