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Cited by 108Neurogenesis and neuroplasticity mechanismsNeuroscience and Neuropharmacology ResearchDevelopmental Biology and Gene Regulation

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New Insights Into Cholinergic Neuron Diversity

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Ahmed, Noorya Yasmin, Knowles, Rhys, Dehorter, Nathalie·2019·Frontiers in Molecular Neuroscience
DOI 10.3389/fnmol.2019.00204PMC PMC6736589
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Abstract

Cholinergic neurons comprise a small population of cells in the striatum but have fundamental roles in fine tuning brain function, and in the etiology of neurological and psychiatric disorders such as Parkinson's disease (PD) or schizophrenia. The process of developmental cell specification underlying neuronal identity and function is an area of great current interest. There has been significant progress in identifying the developmental origins, commonalities in molecular markers, and physiological properties of the cholinergic neurons. Currently, we are aware of a number of key factors that promote cholinergic fate during development. However, the extent of cholinergic cell diversity is still largely underestimated. New insights into the biological basis of their specification indicate that cholinergic neurons may be far more diverse than previously thought. This review article, highlights the physiological features and the synaptic properties that segregate cholinergic cell subtypes. It provides an accurate picture of cholinergic cell diversity underlying their organization and function in neuronal networks. This review article, also discusses current challenges in deciphering the logic of the cholinergic cell heterogeneity that plays a fundamental role in the control of neural processes in health and disease.

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Figure 1 General populations of cholinergic neurons and alterations in disease. (A) Pathologies associated with cholinergic alteration. (B) Three major populations of cholinergic neurons in the brain. Basal forebrain neurons project to higher structures (blue); striatal interneurons project locally throughout the striatum (red); cortical interneurons co-expressing Vasoactive Intestinal Peptide (VIP) and Choline Acetyltransferase (ChAT) project within cortical layers (green). (C) Common properties of cholinergic neurons: aspiny dendrites and a large soma; expression of ChAT, Acetylcholine Esterase (AChE), Vesicular Acetylcholine Transporter (VAChT) expression; tonic firing patterns with a distinct pause in vivo, and a sag in membrane voltage (arrow) in response to hyperpolarizing current (scale: 100 pA).
Figure 1 General populations of cholinergic neurons and alterations in disease. (A) Pathologies associated with cholinergic alteration. (B) Three major populations of cholinergic neurons in the brain. Basal forebrain neurons project to higher structures (blue); striatal interneurons project locally throughout the striatum (red); cortical interneurons co-expressing Vasoactive Intestinal Peptide (VIP) and Choline Acetyltransferase (ChAT) project within cortical layers (green). (C) Common properties of cholinergic neurons: aspiny dendrites and a large soma; expression of ChAT, Acetylcholine Esterase (AChE), Vesicular Acetylcholine Transporter (VAChT) expression; tonic firing patterns with a distinct pause in vivo, and a sag in membrane voltage (arrow) in response to hyperpolarizing current (scale: 100 pA).CC BY · PubMed Central
Figure 2 Developmental diversity in cholinergic neurons. (A) Cholinergic neurons are derived from different embryonic structures. Proliferative zones of an E13.5 mouse brain embryo: Pallium (Pl), Medial Ganglionic Eminence (MGE), Lateral Ganglionic Eminence (LGE), Septal Epithelium (SE), Preoptic Area (POA), and Caudal Ganglionic Eminence (CGE) give rise to cholinergic neurons of different nuclei: Striatum (Str), Cerebral Cortex (Ctx), Nucleus Accumbens (NAc), and the Basal Forebrain: Nucleus Basalis (NB), Medial Septal Nucleus (MSN), Diagonal Band (DB). (B) Genetic diversity in cholinergic interneurons (CINs) in the striatum. Subsets of CINs express Zic4 (blue) and originate from the SE, and Lhx6 (red) and originate from the MGE. Gbx2 is expressed in almost all CINs and preferentially controls development of late-born CINs in the dorsomedial striatum (DMS), but not in early-born CINs in the dorsolateral striatum (DLS). MGE-derived Fgf8 (green) and Fgf17 (purple), and POA-derived Dbx1 (orange) mark three subgroups defined by genetic expression and reliant on developmental origin, but do not account for the entire CIN population (gray).
Figure 2 Developmental diversity in cholinergic neurons. (A) Cholinergic neurons are derived from different embryonic structures. Proliferative zones of an E13.5 mouse brain embryo: Pallium (Pl), Medial Ganglionic Eminence (MGE), Lateral Ganglionic Eminence (LGE), Septal Epithelium (SE), Preoptic Area (POA), and Caudal Ganglionic Eminence (CGE) give rise to cholinergic neurons of different nuclei: Striatum (Str), Cerebral Cortex (Ctx), Nucleus Accumbens (NAc), and the Basal Forebrain: Nucleus Basalis (NB), Medial Septal Nucleus (MSN), Diagonal Band (DB). (B) Genetic diversity in cholinergic interneurons (CINs) in the striatum. Subsets of CINs express Zic4 (blue) and originate from the SE, and Lhx6 (red) and originate from the MGE. Gbx2 is expressed in almost all CINs and preferentially controls development of late-born CINs in the dorsomedial striatum (DMS), but not in early-born CINs in the dorsolateral striatum (DLS). MGE-derived Fgf8 (green) and Fgf17 (purple), and POA-derived Dbx1 (orange) mark three subgroups defined by genetic expression and reliant on developmental origin, but do not account for the entire CIN population (gray).CC BY · PubMed Central
Figure 3 Functional diversity of cholinergic neurons. (A) There is a gradient of baseline activity in striatal CINs along the DMS to ventrolateral (VLS) axis (modified from Matamales et al., 2016 with permission). (B) Two subsets of striatal CINs show morphological and electrophysiological differences. GABAergic CINs (GCIN) have smaller dendritic fields and slower firing rates than purely cholinergic CINs (adapted from Lozovaya et al., 2018 with permission). (C) Basal forebrain cholinergic neurons (CNs) have diverse projection targets and can be grouped into four major categories with subcategories based on collateral targets (adapted from Li et al., 2018 with permission).
Figure 3 Functional diversity of cholinergic neurons. (A) There is a gradient of baseline activity in striatal CINs along the DMS to ventrolateral (VLS) axis (modified from Matamales et al., 2016 with permission). (B) Two subsets of striatal CINs show morphological and electrophysiological differences. GABAergic CINs (GCIN) have smaller dendritic fields and slower firing rates than purely cholinergic CINs (adapted from Lozovaya et al., 2018 with permission). (C) Basal forebrain cholinergic neurons (CNs) have diverse projection targets and can be grouped into four major categories with subcategories based on collateral targets (adapted from Li et al., 2018 with permission).CC BY · PubMed Central

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Metadata

Authors
Ahmed, N. Y., Knowles, R., & Dehorter, N.
Affiliations
Australian National University (AU)
Corresponding author
Dehorter, Nathalie
ORCID
Venue
Frontiers in Molecular Neuroscience
Publisher
Frontiers Media SA
Published
2019-08-27
Volume
12
Pages
204-204
ISSN
1662-5099 (ISSN-L)
DOI
10.3389/fnmol.2019.00204
PMC
PMC6736589
OpenAlex
W2966298191
Cited by
108
References
142
Citations by year
2026: 10 · 2025: 18 · 2024: 23 · 2023: 22 · 2022: 16 · 2021: 12 · 2020: 6 · 2019: 1
FWCI
1.10
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Molecular Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • ANU Open Research (Australian National University) (submittedVersion, cc-by)
Funders
  • Australian National University
  • National Health and Medical Research Council
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
cholinergic neurons, striatum, neuronal specification, synaptic properties, Parkinson's disease, schizophrenia, molecular markers, neuronal networks

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