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Cited by 19Neuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on BehaviorNeurological disorders and treatments

CalDAG-GEFI mediates striatal cholinergic modulation of dendritic excitability, synaptic plasticity and psychomotor behaviors

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Crittenden, Jill R., Zhai, Shenyu, Sauvage, Magdalena, Kitsukawa, Takashi, Burguière, Eric, Thomsen, Morgane, Zhang, Hui, Costa, Cinzia +13 more·2021·Neurobiology of Disease
DOI 10.1016/j.nbd.2021.105473PMC PMC8486000
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Abstract

CalDAG-GEFI (CDGI) is a protein highly enriched in the striatum, particularly in the principal spiny projection neurons (SPNs). CDGI is strongly down-regulated in two hyperkinetic conditions related to striatal dysfunction: Huntington's disease and levodopa-induced dyskinesia in Parkinson's disease. We demonstrate that genetic deletion of CDGI in mice disrupts dendritic, but not somatic, M1 muscarinic receptors (M1Rs) signaling in indirect pathway SPNs. Loss of CDGI reduced temporal integration of excitatory postsynaptic potentials at dendritic glutamatergic synapses and impaired the induction of activity-dependent long-term potentiation. CDGI deletion selectively increased psychostimulant-induced repetitive behaviors, disrupted sequence learning, and eliminated M1R blockade of cocaine self-administration. These findings place CDGI as a major, but previously unrecognized, mediator of cholinergic signaling in the striatum. The effects of CDGI deletion on the self-administration of drugs of abuse and its marked alterations in hyperkinetic extrapyramidal disorders highlight CDGI's therapeutic potential.

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  • Aβ and tau pathology exacerbate vulnerability of cholinergic neurons, while neuroinflammation and mitochondrial dysfunction impair cholinergic energy metabolism and synaptic resilience.

    “For example, Aβ and tau pathology exacerbate the vulnerability of cholinergic neurons, while neuroinflammation and mitochondrial dysfunction impair cholinergic energy metabolism and synaptic resilience [98, 99].”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [99]

    The Discussion’s “Translational implications” section discusses cholinergic signaling and synaptic changes in Huntington’s disease, not Aβ or tau pathology. Searches for those pathologies and for neuroinflammation, mitochondrial dysfunction, and cholinergic energy metabolism found no passage in our copy addressing the claimed mechanisms. No page number is available for the cited passage. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

  • AChEIs donepezil, rivastigmine, and galantamine enhance synaptic ACh availability by delaying enzymatic degradation.

    “Acetylcholinesterase inhibitors (AChEIs), such as donepezil, rivastigmine, and galantamine, which were approved more than two decades ago, enhance synaptic acetylcholine (ACh) availability by delaying its enzymatic degradation.”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [99]

    The Discussion (page unavailable) addresses striatal muscarinic signaling and CDGI, not acetylcholinesterase inhibitors. Searches for donepezil, the three named drugs, and acetylcholine degradation found no passage in our copy supporting their mechanism or approval history. (LLM, conf=0.74)

    Experimental — accuracy not yet measured

  • AChEIs remain the cornerstone of current clinical management, offering modest improvements in cognition, function, and behavior.

    “These drugs remain the cornerstone of current clinical management, offering modest improvements in cognition, function, and behavior [99].”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [99]

    The Discussion (Translational implications; page unavailable) discusses muscarinic receptor antagonists for Parkinson’s motor symptoms, not acetylcholinesterase inhibitors. Searches for AChEIs and for improvements in cognition, function, and behavior found no passage in our copy addressing the claimed clinical benefits or cornerstone status. (LLM, conf=0.76)

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Authors
Crittenden, J. R., Zhai, S., Sauvage, M., Kitsukawa, T., Burguière, E., Thomsen, M., Zhang, H., Costa, C., Martella, G., Ghiglieri, V., Picconi, B., Pescatore, K. A., Unterwald, E. M., Jackson, W. S., Housman, D. E., Caine, S. B., Sulzer, D., Calabresi, P., Smith, A. C., Surmeier, D. J., & Graybiel, A. M.
Affiliations
  • McGovern Institute for Brain Research (US)
  • Northwestern University (US)
  • The University of Osaka (JP)
  • Centre National de la Recherche Scientifique (FR)
  • University of Copenhagen (DK)
  • Thomas Jefferson University (US)
  • University of Perugia (IT)
  • Fondazione Santa Lucia (IT)
  • Vita-Salute San Raffaele University (IT)
  • Istituti di Ricovero e Cura a Carattere Scientifico (IT)
  • Temple University (US)
  • Linköping University (SE)
  • Koch Institute for Integrative Cancer Research At MIT (US)
  • Harvard University (US)
  • New York State Psychiatric Institute (US)
  • Università Cattolica del Sacro Cuore (IT)
  • University of Arizona (US)
Corresponding author
Graybiel, Ann M.
ORCID
Venue
Neurobiology of Disease
Publisher
Elsevier BV
Published
2021-10
Volume
158
Pages
105473
ISSN
0969-9961 (ISSN-L)
DOI
10.1016/j.nbd.2021.105473
PMC
PMC8486000
OpenAlex
W3189374286
Cited by
19
References
4
Citations by year
2026: 4 · 2025: 6 · 2024: 2 · 2023: 3 · 2022: 4
FWCI
1.04
Type
journal article
Language
en
Open access
Licence
Locations
  • Neurobiology of Disease (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion, other-oa)
  • PubMed Central (acceptedVersion, cc-by-nc-nd)
  • The Medicine Forum (submittedVersion, cc-by-nc-nd)
  • Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
  • DiVA (Linkoping University) (submittedVersion, other-oa)
  • HAL (submittedVersion, other-oa)
  • HAL (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
  • Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by-nc-nd)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion, other-oa)
  • Zenodo (CERN European Organization for Nuclear Research) (cc-by)
Funders
  • Simons Foundation
  • Stanley Medical Research Institute
  • JPB Foundation
  • Broad Institute
  • European Commission (222918)
  • Stanley Center for Psychiatric Research, Broad Institute
  • National Institute on Aging (R01AG050548)
  • National Institute of Mental Health (MH 071847, F32MH065815, R01MH071847)
  • National Institute on Drug Abuse (DA07418, DA027825, MH071847, R00DA027825, R01DA007418)
  • National Institute of Neurological Disorders and Stroke (R37NS034696)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R37HD028341)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Health Sciences › Medicine › Neurology › Neurological disorders and treatments
Keywords
CalDAG-GEFI, striatum, cholinergic neurotransmission, M1 muscarinic receptor, indirect pathway, dendritic excitability, excitatory postsynaptic potentials, long-term potentiation, synaptic plasticity, psychomotor behavior, cocaine self-administration, sequence learning, Huntington's disease, levodopa-induced dyskinesia, hyperkinetic disorder, extrapyramidal disorders
MeSH terms
Central Nervous System Stimulants, Animals, Basal Ganglia Diseases, Dendrites, Hyperkinesis, Male, Motor Activity, Neuronal Plasticity, Parasympathetic Nervous System, Synapses, Neostriatum, Long-Term Potentiation, Mice, Knockout, Excitatory Postsynaptic Potentials, Substance-Related Disorders, Polymorphism, Single Nucleotide, Guanine Nucleotide Exchange Factors, Receptor, Muscarinic M1, Mice

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