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PMID: 25855185 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons.

Delevich K, Tucciarone J, Huang ZJ, Li B

Abstract

Although the medial prefrontal cortex (mPFC) is classically defined by its reciprocal connections with the mediodorsal thalamic nucleus (MD), the nature of information transfer between MD and mPFC is poorly understood. In sensory thalamocortical pathways, thalamic recruitment of feedforward inhibition mediated by fast-spiking, putative parvalbumin-expressing (PV) interneurons is a key feature that enables cortical neurons to represent sensory stimuli with high temporal fidelity. Whether a similar circuit mechanism is in place for the projection from the MD (a higher-order thalamic nucleus that does not receive direct input from the periphery) to the mPFC is unknown. Here we show in mice that inputs from the MD drive disynaptic feedforward inhibition in the dorsal anterior cingulate cortex (dACC) subregion of the mPFC. In particular, we demonstrate that axons arising from MD neurons directly synapse onto and excite PV interneurons that in turn mediate feedforward inhibition of pyramidal neurons in layer 3 of the dACC. This feedforward inhibition in the dACC limits the time window during which pyramidal neurons integrate excitatory synaptic inputs and fire action potentials, but in a manner that allows for greater flexibility than in sensory cortex. These findings provide a foundation for understanding the role of MD-PFC circuit function in cognition.

Keywords
anterior cingulate cortex feedforward inhibition medial prefrontal cortex mediodorsal thalamus parvalbumin interneuron
MeSH Terms
Afferent Pathways/physiology Animals Channelrhodopsins DNA-Binding Proteins/genetics,metabolism Dependovirus/genetics Excitatory Amino Acid Agonists/pharmacology GABA Antagonists/pharmacology Gyrus Cinguli/cytology In Vitro Techniques Luminescent Proteins/genetics,metabolism Mediodorsal Thalamic Nucleus/physiology Mice Mice, Inbred C57BL Mice, Transgenic Neural Inhibition/physiology Neurons/physiology Parvalbumins/genetics,metabolism Picrotoxin/pharmacology RNA, Untranslated/genetics,metabolism Synaptic Potentials/drug effects Transcription Factors/genetics,metabolism Transduction, Genetic
Chemicals
Channelrhodopsins DNA-Binding Proteins Excitatory Amino Acid Agonists GABA Antagonists Grhl3 protein, mouse Gt(ROSA)26Sor non-coding RNA, mouse Luminescent Proteins Parvalbumins RNA, Untranslated Transcription Factors Picrotoxin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Delevich Kristen
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, Watson School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, and.
Tucciarone Jason
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, MSTP/Neuroscience Graduate Program, Stony Brook University, Stony Brook, New York 11790.
Huang Z Josh
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, Watson School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, and.
Li Bo ORCID
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, Watson School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, and [email protected].
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Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2015-04-08
Pages
5743-53
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC4388929
Subset
IM
Grants
NIMH NIH HHS · R01 MH101214 · United States
NIGMS NIH HHS · T32 GM065094 · United States
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