Cholinergic modulation of striatal microcircuits

The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, com...

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Published inThe European journal of neuroscience Vol. 49; no. 5; pp. 604 - 622
Main Authors Abudukeyoumu, Nilupaer, Hernandez‐Flores, Teresa, Garcia‐Munoz, Marianela, Arbuthnott, Gordon W.
Format Journal Article
LanguageEnglish
Published France Wiley Subscription Services, Inc 01.03.2019
John Wiley and Sons Inc
Subjects
acetylcholine
Acetylcholine receptors (muscarinic)
Acetylcholine receptors (nicotinic)
cholinergic interneurons
Dystonia
Ibags Special Issue
Innervation
Interneurons
Movement disorders
Neostriatum
Neurodegenerative diseases
Neurological diseases
Neuromodulation
Parkinson's disease
Special Issue Review
Spiny neurons
striatum
Synaptic plasticity
neuromodulation
cholinergic interneurons
acetylcholine
striatum
Online AccessGet full text
ISSN0953-816X
1460-9568
1460-9568
DOI10.1111/ejn.13949

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Abstract The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, compared to other brain regions, is the cholinergic interneurons. These interneurons provide an extensive local innervation that suggests they may be a key modulator of striatal microcircuits. Supporting this idea requires the consideration of functional properties of these interneurons, their influence on medium spiny neurons, other interneurons, and interactions with other synaptic regulators. Here, we underline the effects of intrastriatal and extrastriatal afferents onto cholinergic interneurons and discuss the activation of pre‐ and postsynaptic muscarinic and nicotinic receptors that participate in the modulation of intrastriatal neuronal interactions. We further address recent findings about corelease of other transmitters in cholinergic interneurons and actions of these interneurons in striosome and matrix compartments. In addition, we summarize recent evidence on acetylcholine‐mediated striatal synaptic plasticity and propose roles for cholinergic interneurons in normal striatal physiology. A short examination of their role in neurological disorders such as Parkinson's, Huntington's, and Tourette's pathologies and dystonia is also included. We review literature on striatal cholinergic interneurons: their synaptic and non‐synaptic release, afferents, and connectivity with the activation of pre‐ and postsynaptic cholinergic receptors and their role in the modulation of normal and pathological microcircuits. Drawings illustrate glutamatergic and dopaminergic afferents and magnified microcircuit with cholinergic interneuron (red) surrounded by GABAergic interneurons (different colors) and medium spiny neurons (green).
AbstractList The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, compared to other brain regions, is the cholinergic interneurons. These interneurons provide an extensive local innervation that suggests they may be a key modulator of striatal microcircuits. Supporting this idea requires the consideration of functional properties of these interneurons, their influence on medium spiny neurons, other interneurons, and interactions with other synaptic regulators. Here, we underline the effects of intrastriatal and extrastriatal afferents onto cholinergic interneurons and discuss the activation of pre- and postsynaptic muscarinic and nicotinic receptors that participate in the modulation of intrastriatal neuronal interactions. We further address recent findings about corelease of other transmitters in cholinergic interneurons and actions of these interneurons in striosome and matrix compartments. In addition, we summarize recent evidence on acetylcholine-mediated striatal synaptic plasticity and propose roles for cholinergic interneurons in normal striatal physiology. A short examination of their role in neurological disorders such as Parkinson's, Huntington's, and Tourette's pathologies and dystonia is also included.The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, compared to other brain regions, is the cholinergic interneurons. These interneurons provide an extensive local innervation that suggests they may be a key modulator of striatal microcircuits. Supporting this idea requires the consideration of functional properties of these interneurons, their influence on medium spiny neurons, other interneurons, and interactions with other synaptic regulators. Here, we underline the effects of intrastriatal and extrastriatal afferents onto cholinergic interneurons and discuss the activation of pre- and postsynaptic muscarinic and nicotinic receptors that participate in the modulation of intrastriatal neuronal interactions. We further address recent findings about corelease of other transmitters in cholinergic interneurons and actions of these interneurons in striosome and matrix compartments. In addition, we summarize recent evidence on acetylcholine-mediated striatal synaptic plasticity and propose roles for cholinergic interneurons in normal striatal physiology. A short examination of their role in neurological disorders such as Parkinson's, Huntington's, and Tourette's pathologies and dystonia is also included.
The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, compared to other brain regions, is the cholinergic interneurons. These interneurons provide an extensive local innervation that suggests they may be a key modulator of striatal microcircuits. Supporting this idea requires the consideration of functional properties of these interneurons, their influence on medium spiny neurons, other interneurons, and interactions with other synaptic regulators. Here, we underline the effects of intrastriatal and extrastriatal afferents onto cholinergic interneurons and discuss the activation of pre‐ and postsynaptic muscarinic and nicotinic receptors that participate in the modulation of intrastriatal neuronal interactions. We further address recent findings about corelease of other transmitters in cholinergic interneurons and actions of these interneurons in striosome and matrix compartments. In addition, we summarize recent evidence on acetylcholine‐mediated striatal synaptic plasticity and propose roles for cholinergic interneurons in normal striatal physiology. A short examination of their role in neurological disorders such as Parkinson's, Huntington's, and Tourette's pathologies and dystonia is also included.
The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction demonstrated with the use of newly available tools. It is well known that the main source of the high level of acetylcholine in the striatum, compared to other brain regions, is the cholinergic interneurons. These interneurons provide an extensive local innervation that suggests they may be a key modulator of striatal microcircuits. Supporting this idea requires the consideration of functional properties of these interneurons, their influence on medium spiny neurons, other interneurons, and interactions with other synaptic regulators. Here, we underline the effects of intrastriatal and extrastriatal afferents onto cholinergic interneurons and discuss the activation of pre‐ and postsynaptic muscarinic and nicotinic receptors that participate in the modulation of intrastriatal neuronal interactions. We further address recent findings about corelease of other transmitters in cholinergic interneurons and actions of these interneurons in striosome and matrix compartments. In addition, we summarize recent evidence on acetylcholine‐mediated striatal synaptic plasticity and propose roles for cholinergic interneurons in normal striatal physiology. A short examination of their role in neurological disorders such as Parkinson's, Huntington's, and Tourette's pathologies and dystonia is also included. We review literature on striatal cholinergic interneurons: their synaptic and non‐synaptic release, afferents, and connectivity with the activation of pre‐ and postsynaptic cholinergic receptors and their role in the modulation of normal and pathological microcircuits. Drawings illustrate glutamatergic and dopaminergic afferents and magnified microcircuit with cholinergic interneuron (red) surrounded by GABAergic interneurons (different colors) and medium spiny neurons (green).
Author Abudukeyoumu, Nilupaer
Arbuthnott, Gordon W.
Hernandez‐Flores, Teresa
Garcia‐Munoz, Marianela
AuthorAffiliation 1 Okinawa Institute of Science and Technology Graduate University Okinawa Japan
AuthorAffiliation_xml – name: 1 Okinawa Institute of Science and Technology Graduate University Okinawa Japan
Author_xml – sequence: 1
  givenname: Nilupaer
  surname: Abudukeyoumu
  fullname: Abudukeyoumu, Nilupaer
  organization: Okinawa Institute of Science and Technology Graduate University
– sequence: 2
  givenname: Teresa
  surname: Hernandez‐Flores
  fullname: Hernandez‐Flores, Teresa
  organization: Okinawa Institute of Science and Technology Graduate University
– sequence: 3
  givenname: Marianela
  surname: Garcia‐Munoz
  fullname: Garcia‐Munoz, Marianela
  organization: Okinawa Institute of Science and Technology Graduate University
– sequence: 4
  givenname: Gordon W.
  surname: Arbuthnott
  fullname: Arbuthnott, Gordon W.
  email: gordon@oist.jp
  organization: Okinawa Institute of Science and Technology Graduate University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29797362$$D View this record in MEDLINE/PubMed
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Issue 5
Keywords neuromodulation
cholinergic interneurons
acetylcholine
striatum
Language English
License Attribution
2018 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Edited by Paul Bolam. Reviewed by Paul Apiella, Jose Bargas and Margaret E. Rice.
N.A. and T.H.‐F. contributed equally to this work.
All peer review communications can be found with the online version of the article.
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SSID ssj0008645
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SecondaryResourceType review_article
Snippet The purpose of this review is to bridge the gap between earlier literature on striatal cholinergic interneurons and mechanisms of microcircuit interaction...
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SubjectTerms acetylcholine
Acetylcholine receptors (muscarinic)
Acetylcholine receptors (nicotinic)
cholinergic interneurons
Dystonia
Ibags Special Issue
Innervation
Interneurons
Movement disorders
Neostriatum
Neurodegenerative diseases
Neurological diseases
Neuromodulation
Parkinson's disease
Special Issue Review
Spiny neurons
striatum
Synaptic plasticity
Title Cholinergic modulation of striatal microcircuits
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fejn.13949
https://www.ncbi.nlm.nih.gov/pubmed/29797362
https://www.proquest.com/docview/2193929139
https://www.proquest.com/docview/2045269449
https://pubmed.ncbi.nlm.nih.gov/PMC6587740
Volume 49
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