The DOI matches its Crossref record; 39 of the 39 references it cites were found in a registry or an index.
Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: synaptic pattern and age-related atrophy
Abstract
This study addresses the issue of whether cholinergic varicosities in the cerebral cortex establish 'classical synapses' or whether they communicate with their targets non-synaptically by 'volume transmission'. Most recent studies in the neocortex have suggested that acetylcholine acts non-synaptically, however in the present study we provide ultrastructural evidence that suggests synaptic mechanisms prevail. This conclusion is based upon our ultrastructural observations that cholinergic boutons--as revealed by immunoreactivity for the specific cholinergic market, vesicular acetylcholine transporter--establish a high percentage of classical synapses in layer V of the rat parietal cortex. Furthermore, the combination of this approach with the intracellular labeling of large pyramidal neurons on slice preparations revealed significant incidences of cholinergic contacts abutting preferentially on dendritic shafts. Finally, we have gathered information suggesting that cholinergic boutons undergo atrophy with aging which could be related to the well-known cholinergic and cognitive decline. These results illustrate that the cholinergic terminations in the neocortex establish proper synaptic connections and that they experience important age-dependent atrophy.
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“Anatomical studies have identified cortical cholinergic synapses that are structurally similar to those of other point-to-point neurotransmitters, in both rats (Turrini et al., 2001) and humans (Smiley et al., 1997).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Turrini et al., 2001
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Cites
The cholinergic hypothesis of geriatric memory dysfunction
Bartus, R. T., Dean, R. L., Beer, B., & Lippa, A. S. (1982) · Science · doi:10.1126/science.7046051 · Cited by 5,545
Alzheimer's Disease: A Disorder of Cortical Cholinergic Innervation
Coyle, J. T., Price, D. L., & DeLong, M. R. (1983) · Science · doi:10.1126/science.6338589 · Cited by 3,052
Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6)
Mesulam, M. M., Mufson, E. J., Wainer, B. H., & Levey, A. I. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90108-2 · Cited by 2,329
Alzheimer disease: Evidence for selective loss of cholinergic neurons in the nucleus basalis
Whitehouse, P. J., Price, D. L., Clark, A. W., Coyle, J. T., & DeLong, M. R. (1981) · Annals of Neurology · doi:10.1002/ana.410100203 · Cited by 1,736
Wada, E., Wada, K., Boulter, J., Deneris, E. S., Heinemann, S., Patrick, J., & Swanson, L. W. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902840212 · Cited by 1,044
Fischer, W., Wictorin, K., Björklund, A., Williams, L., Varon, S. S., & Gage, F. H. (1987) · Nature · doi:10.1038/329065a0 · Cited by 1,024
DeFelipe, J., & Fariñas, I. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90015-7 · Cited by 975
Acetylcholine in mind: a neurotransmitter correlate of consciousness?
Perry, E. K., Walker, M. P., Grace, J., & Perry, R. H. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01361-7 · Cited by 764
Cognitive functions of cortical acetylcholine: toward a unifying hypothesis
Sarter, M. F., & Bruno, J. P. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(96)00009-4 · Cited by 675
Mechanisms of action of acetylcholine in the guinea‐pig cerebral cortex in vitro.
McCormick, D. A., & Prince, D. A. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016112 · Cited by 499
Research works printed but not linked: 2
- Marchese, 1998, Age-related depletion of cholinergic synapses in the rat cerebral cortex, Soc. Neurosci. Abstr., 24, 1493
- Ribeiro-da-Silva, A., Priestley, J.V., Cuello, A.C., 1993. Pre-embedding ultrastructural immunocytochemistry. In: Cuello, A.C. (Ed.), Immunohistochemistry II. Wiley, Chichester, pp. 181–227.
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Metadata
- Authors
- Turrini, P., Casu, M. A., Wong, T. P., De Koninck, Y., Ribeiro-da-Silva, A., & Cuello, A. C.
- Affiliations
- McGill University (CA)
- Corresponding author
- Cuello, A.C
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2001-07
- Volume
- 105
- Issue
- 2
- Pages
- 277-285
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2045697035
- Cited by
- 135
- References
- 39
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 5 · 2020: 6 · 2019: 1 · 2018: 5 · 2017: 2 · 2016: 2 · 2015: 6 · 2014: 8 · 2013: 11 · 2012: 9
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- P-arch (Science and Technology Park of Sardinia) (submittedVersion)
- Funders
- National Institutes of Health (5r01ns034022-03)
- National Institute of Neurological Disorders and Stroke (NS 34022)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Pharmacology (medical) › Cholinesterase and Neurodegenerative Diseases
- Keywords
- cholinergic nerve terminals, volume transmission, acetylcholine, vesicular acetylcholine transporter, parietal cortex, layer V, pyramidal neurons, dendritic synapses, synaptic ultrastructure, cognitive decline
- MeSH terms
- Acetylcholine, Aging, Animals, Atrophy, Carrier Proteins, Cerebral Cortex, Cholinergic Fibers, Dendrites, Image Processing, Computer-Assisted, Immunohistochemistry, Male, Microscopy, Electron, Rats, Inbred F344, Presynaptic Terminals, Pyramidal Cells, Patch-Clamp Techniques, Membrane Transport Proteins, Vesicular Transport Proteins, Vesicular Acetylcholine Transport Proteins, Rats
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