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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Anatomical studies have identified cortical cholinergic synapses that are structurally similar to those of other point-to-point neurotransmitters, in both rats and humans.
“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
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 · see citing works
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 3,050 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Fischer, W., Wictorin, K., Björklund, A., Williams, L., Varon, S. S., & Gage, F. H. (1987) · Nature · doi:10.1038/329065a0 · Cited by 1,024 · see citing works
DeFelipe, J., & Fariñas, I. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90015-7 · Cited by 975 · see citing works
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 · see citing works
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 662 · see citing works
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 · see citing works
Aging, Alzheimer's disease, and the cholinergic system of the basal forebrain
McGeer, P. L., McGeer, E. G., Suzuki, J., DOLMAN, C. E., & Nagai, T. (1984) · Neurology · doi:10.1212/wnl.34.6.741 · Cited by 457 · see citing works
Cholinergic Switching Within Neocortical Inhibitory Networks
Xiang, Z., Huguenard, J. R., & Prince, D. A. (1998) · Science · doi:10.1126/science.281.5379.985 · Cited by 438 · see citing works
Diffuse transmission by acetylcholine in the CNS
Descarries, L., Gisiger, V., & Steriade, M. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00050-6 · Cited by 406 · see citing works
Houser, C. R., Crawford, G. D., Salvaterra, P. M., & Vaughn, J. E. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902340103 · Cited by 395 · see citing works
Levey, A. I. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13541 · Cited by 359 · see citing works
Eckenstein, F., & Baughman, R. W. (1984) · Nature · doi:10.1038/309153a0 · Cited by 356 · see citing works
An anatomical study of cholinergic innervation in rat cerebral cortex
Eckenstein, F. P., Baughman, R. P., & Quinn, J. F. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90251-5 · Cited by 348 · see citing works
Two types of muscarinic response to acetylcholine in mammalian cortical neurons.
McCormick, D. A., & Prince, D. A. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.18.6344 · Cited by 302 · see citing works
Weihe, E., Tao-Cheng, J.-H., Schäfer, M., Erickson, J. D., & Eiden, L. E. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3547 · Cited by 301 · see citing works
Gilmor, M. L., Nash, N. R., Roghani, A., Edwards, R., Yi, H. L., Hersch, S. M., & Levey, A. I. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-07-02179.1996 · Cited by 283 · see citing works
van der Zee, E. A., & Luiten, P. G. M. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00092-6 · Cited by 261 · see citing works
Mrzljak, L., Levey, A. I., & Goldman-Rakic, P. S. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.11.5194 · Cited by 256 · see citing works
Role of Neurotrophins in Synapse Development and Plasticity
Lu, B., & Figurov, A. (1997) · Reviews in the Neurosciences · doi:10.1515/revneuro.1997.8.1.1 · Cited by 241 · see citing works
Testa, C. M., Friberg, I. K., Weiss, S. W., & Standaert, D. G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980105)390:1 · Cited by 237 · see citing works
Synaptic plasticity in cortical systems
Klintsova, A. Y., & Greenough, W. T. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80028-2 · Cited by 237 · see citing works
Umbriaco, D., Watkins, K. C., Descarries, L., Cozzari, C., & Hartman, B. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903480304 · Cited by 237 · see citing works
Nerve growth factor-induced synaptogenesis and hypertrophy of cortical cholinergic terminals.
Garofalo, L., Ribeiro‐da‐Silva, A., & Cuello, A. C. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.7.2639 · Cited by 163 · see citing works
Self-citationSeizures, memory and synaptic plasticity
Reid, I., & Stewart, C. A. (1997) · Seizure · doi:10.1016/s1059-1311(97)80034-9 · Cited by 137 · see citing works
Hellweg, R., Fischer, W., Hock, C., Gage, F. H., Björklund, A., & Thoenen, H. (1990) · Brain Research · doi:10.1016/0006-8993(90)90348-f · Cited by 135 · see citing works
Beaulieu, C., & Somogyi, P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040412 · Cited by 126 · see citing works
Debeir, T., Saragovi, H. U., & Cuello, A. C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.4067 · Cited by 114 · see citing works
Self-citationRylett, R. J., Goddard, S., Schmidt, B., & Williams, L. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03956.1993 · Cited by 101 · see citing works
Morphological and electrophysiological characteristics of pyramidal tract neurons in the rat
Landry, P., Wilson, C. J., & Kitai, S. T. (1984) · Experimental Brain Research · doi:10.1007/bf00231144 · Cited by 94 · see citing works
de Lima, A. D., & Singer, W. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902500306 · Cited by 92 · see citing works
Cholinergic synaptic circuitry in the macaque prefrontal cortex
Mrzijak, L., Pappy, M., Léránth, C., & Goldman, P. S. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903570409 · Cited by 92 · see citing works
Postsynaptic actin and neuronal plasticity
Matus, A. I. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00018-5 · Cited by 82 · see citing works
Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections
Smiley, J. F., Morrell, F., & Mesulam, M. M. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6413 · Cited by 79 · see citing works
Roghani, A., Shirzadi, A., Butcher, L. L., & Edwards, R. H. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00291-1 · Cited by 70 · see citing works
Aoki, C. J., & Kabak, S. (1992) · Visual Neuroscience · doi:10.1017/s0952523800002832 · Cited by 68 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
Nicotinic Acetylcholine Receptors and Nicotinic Cholinergic Mechanisms of the Central Nervous System
Dani, J. A., & Bertrand, D. (2007) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.47.120505.105214 · Cited by 1,197 · see citing works
Nicotinic acetylcholine receptors: from structure to brain function
Hogg, R. C., Raggenbass, M., & Bertrand, D. (2003) · Springer eBooks · doi:10.1007/s10254-003-0005-1 · Cited by 529 · see citing works
Phasic acetylcholine release and the volume transmission hypothesis: time to move on
Sarter, M. F., Parikh, V., & Howe, W. M. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2635 · Cited by 340 · see citing works
Parsons, C. G., Danysz, W., Dekundy, A., & Pulte, I. (2013) · Neurotoxicity Research · doi:10.1007/s12640-013-9398-z · Cited by 337 · see citing works
Gain Modulation by Nicotine in Macaque V1
Disney, A. A., Aoki, C., & Hawken, M. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.034 · Cited by 331 · see citing works
Cholinergic function and Alzheimer's disease
Giacobini, E. (2003) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.935 · Cited by 284 · see citing works
Henny, P., & Jones, B. E. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06029.x · Cited by 266 · see citing works
Modulators in concert for cognition: Modulator interactions in the prefrontal cortex
Briand, L. A., Gritton, H., Howe, W. M., Young, D. A., & Sarter, M. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.06.007 · Cited by 216 · see citing works
Yamasaki, M., Matsui, M., & Watanabe, M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5719-09.2010 · Cited by 203 · see citing works
Nicotinic modulation of neuronal networks: from receptors to cognition
Mansvelder, H. D., van Aerde, K. I., Couey, J. J., & Brussaard, A. B. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0070-z · Cited by 201 · see citing works
Nicotinic α7 receptors: Synaptic options and downstream signaling in neurons
Berg, D. K., & Conroy, W. G. (2002) · Journal of Neurobiology · doi:10.1002/neu.10116 · Cited by 198 · see citing works
Alkondon, M., & Albuquerque, E. X. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)45007-3 · Cited by 197 · see citing works
Heterogeneity of phasic cholinergic signaling in neocortical neurons
Gulledge, A. T., Park, S. B., Kawaguchi, Y., & Stuart, G. J. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00493.2006 · Cited by 194 · see citing works
Nelson, A., & MOONEY, R. D. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.031 · Cited by 190 · see citing works
Layer- and Cell Type-Specific Modulation of Excitatory Neuronal Activity in the Neocortex
Radnikow, G., & Feldmeyer, D. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00001 · Cited by 180 · see citing works
Cholinergic Inhibition of Neocortical Pyramidal Neurons
Gulledge, A. T., & Stuart, G. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2697-05.2005 · Cited by 182 · see citing works
Co-transmission of acetylcholine and GABA regulates hippocampal states
Takács, V. T., Cserép, C., Schlingloff, D., Pósfai, B., Szőnyi, A., Sos, K. E., Környei, Z., Dénes, Á., Gulyás, A. I., Freund, T. F., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05136-1 · Cited by 169 · see citing works
Spikes, synchrony, and attentive learning by laminar thalamocortical circuits
Grossberg, S., & Massimiliano Versace, A. (2008) · Brain Research · doi:10.1016/j.brainres.2008.04.024 · Cited by 158 · see citing works
Basal forebrain cholinergic signalling: development, connectivity and roles in cognition
Ananth, M. R., Rajebhosale, P., Kim, R., Talmage, D. A., & Role, L. W. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00677-x · Cited by 148 · see citing works
Kawai, H., Zago, W., & Berg, D. K. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07903.2002 · Cited by 140 · see citing works
Arroyo, S., Bennett, C., Aziz, D., Brown, S. P., & Hestrin, S. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0115-12.2012 · Cited by 138 · see citing works
Nonsynaptic Chemical Transmission Through Nicotinic Acetylcholine Receptors
Lendvai, B., & Vizi, E. S. (2008) · Physiological Reviews · doi:10.1152/physrev.00040.2006 · Cited by 137 · see citing works
Nerve growth factor metabolic dysfunction in Alzheimer's disease and Down syndrome
Iulita, M. F., & Cuello, A. C. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.04.010 · Cited by 135 · see citing works
Self-citationCellular, Synaptic and Network Effects of Acetylcholine in the Neocortex
Colangelo, C., Shichkova, P., Keller, D. X., Markram, H., & Ramaswamy, S. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00024 · Cited by 134 · see citing works
Acetylcholine Dynamically Controls Spatial Integration in Marmoset Primary Visual Cortex
Roberts, M. J., Zinke, W., Guo, K., Robertson, R., McDonald, J. S., & Thiele, A. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00911.2004 · Cited by 127 · see citing works
Spatiotemporal specificity in cholinergic control of neocortical function
Muñoz, W., & Rudy, B. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.02.015 · Cited by 122 · see citing works
Impact of Basal Forebrain Cholinergic Inputs on Basolateral Amygdala Neurons
Ünal, Ç. T., Paré, D., & Záborszky, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2706-14.2015 · Cited by 124 · see citing works
Trueta, C., & De‐Miguel, F. F. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00319 · Cited by 122 · see citing works
Hu, M. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2002.1202 · Cited by 117 · see citing works
Nicotinic Acetylcholine Receptors in Sensory Cortex: Figure 1
Metherate, R. (2004) · Learning & Memory · doi:10.1101/lm.69904 · Cited by 116 · see citing works
Neuronal Substrates of Sleep and Epilepsy
Steriade, M. (2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541711 · Cited by 116 · see citing works
Forebrain Cholinergic Signaling: Wired and Phasic, Not Tonic, and Causing Behavior
Sarter, M. F., & Lustig, C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1305-19.2019 · Cited by 110 · see citing works
Towart, L. A., Alves, S. E., Znamensky, V., Hayashi, S., McEwen, B. S., & Milner, T. A. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10753 · Cited by 109 · see citing works
Impact of the NGF Maturation and Degradation Pathway on the Cortical Cholinergic System Phenotype
Allard, S., León, W., Pakavathkumar, P., Bruno, M. A., Ribeiro‐da‐Silva, A., & Cuello, A. C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1144-11.2012 · Cited by 101 · see citing works
Self-citationDisney, A. A., Domakonda, K. V., & Aoki, C. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21096 · Cited by 99 · see citing works
The role of nicotinic acetylcholine receptors in autosomal dominant nocturnal frontal lobe epilepsy
Becchetti, A., Aracri, P., Meneghini, S., Brusco, S., & Amadeo, A. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00022 · Cited by 102 · see citing works
Bruno, M. A., Clarke, P. B. S., Seltzer, A. M., Quirion, R., Burgess, K., Cuello, A. C., & Saragovi, H. U. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1508-04.2004 · Cited by 89 · see citing works
Self-citationMechanisms Generating Dual-Component Nicotinic EPSCs in Cortical Interneurons
Bennett, C., Arroyo, S., Berns, D. S., & Hestrin, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3565-12.2012 · Cited by 80 · see citing works
Targeting α7 Nicotinic Acetylcholine Receptors in the Treatment of Schizophrenia
Hajós, M., & Rogers, B. N. (2010) · Current Pharmaceutical Design · doi:10.2174/138161210790361434 · Cited by 73 · see citing works
Diverse Spatiotemporal Scales of Cholinergic Signaling in the Neocortex
Disney, A. A., & Higley, M. J. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1306-19.2019 · Cited by 71 · see citing works
Luchicchi, A., Bloem, B., Viaña, J. N. M., Mansvelder, H. D., & Role, L. W. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00024 · Cited by 70 · see citing works
Nicotinic modulation of cortical circuits
Arroyo, S., Bennett, C., & Hestrin, S. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00030 · Cited by 64 · see citing works
Alzheimers Disease and Neural Transplantation as Prospective Cell Therapy
de Oliveira, A. A., & Hodges, H. R. (2005) · Current Alzheimer Research · doi:10.2174/1567205052772759 · Cited by 64 · see citing works
Distribution and effects of the muscarinic receptor subtypes in the primary visual cortex
Groleau, M., Kang, J. I., Huppé‐Gourgues, F., & Vaucher, E. (2015) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00010 · Cited by 60 · see citing works
Aracri, P., Consonni, S., Morini, R., Perrella, M., Rodighiero, S., Amadeo, A., & Becchetti, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp214 · Cited by 60 · see citing works
Ultrastructural features of the acetylcholine innervation in the developing parietal cortex of rat
Mechawar, N., Watkins, K. C., & Descarries, L. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10114 · Cited by 58 · see citing works
Neuroligin 2 Is Expressed in Synapses Established by Cholinergic Cells in the Mouse Brain
Takács, V. T., Freund, T. F., & Nyíri, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072450 · Cited by 56 · see citing works
Acetylcholine release and inhibitory interneuron activity in hippocampal CA1
McQuiston, A. R. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00020 · Cited by 55 · see citing works
A transgenic mouse model reveals fast nicotinic transmission in hippocampal pyramidal neurons
Grybko, M. J., Hahm, E.-T., Perrine, W., Parnes, J. A., Chick, W. S. H., Sharma, G., Finger, T. E., & Vijayaraghavan, S. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07671.x · Cited by 53 · see citing works
Hay, Y. A., Lambolez, B., & Tricoire, L. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv085 · Cited by 51 · see citing works
Lucas-Meunier, E., Monier, C., Amar, M., Baux, G., Frégnac, Y., & Fossier, P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn258 · Cited by 51 · see citing works
Poorthuis, R. B., & Mansvelder, H. D. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.003 · Cited by 48 · see citing works
Bell, L. A., Bell, K. A., & McQuiston, A. R. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.026 · Cited by 48 · see citing works
Coppola, J. J., & Disney, A. A. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00008 · Cited by 48 · see citing works
Dasgupta, R., Seibt, F., & Beierlein, M. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0566-18.2018 · Cited by 47 · see citing works
Zolles, G., Wagner, E., Lampert, A., & Sutor, B. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn158 · Cited by 42 · see citing works
Francis, P. T., Parsons, C. G., & Jones, R. W. (2012) · Expert Review of Neurotherapeutics · doi:10.1586/ern.12.124 · Cited by 45 · see citing works
Mäki‐Marttunen, T., & Mäki-Marttunen, V. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010506 · Cited by 44 · see citing works
Esmaeilzade, B., Nobakht, M., Joghataei, M. T., Rahbar‐Roshandel, N., Rasouli, H., Samadikuchaksaraei, A., Hosseini, S. M., Najafzadeh, N., Asalgoo, S., Hejazian, L. B., et al. (1996) · Europe PMC (PubMed Central) · doi:10.6091/ibj.1029.2012 · Cited by 42 · see citing works
Majdi, M., Ribeiro‐da‐Silva, A., & Cuello, A. C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05966.x · Cited by 42 · see citing works
Self-citationGiuliano, C., Parikh, V., Ward, J. R., Chiamulera, C., & Sarter, M. (2008) · Neurochemistry International · doi:10.1016/j.neuint.2008.02.002 · Cited by 41 · see citing works
Localisation of the high-affinity choline transporter-1 in the rat skeletal motor unit
Lips, K. S., Pfeil, U., Haberberger, R. V., & Kummer, W. (2002) · Cell and Tissue Research · doi:10.1007/s00441-002-0520-4 · Cited by 41 · see citing works
Disney, A. A., & Reynolds, J. H. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23456 · Cited by 40 · see citing works
“In the neocortex, ACh is usually released from varicosities that are not apposed to a synaptic specialization (Aoki and Kabak, 1992; Beaulieu and Somogyi, 1991; Umbriaco et al., 1994), a mode of release known as volume transmission (but see Turrini et al., 2001).”
BackgroundAnisuzzaman, A. S. M., Uwada, J., Masuoka, T., Yoshiki, H., Nishio, M., Ikegaya, Y., Takahashi, N., Matsuki, N., Fujibayashi, Y., Yonekura, Y., et al. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12306 · Cited by 39 · see citing works
ERK-mediated NGF signaling in the rat septo-hippocampal pathway diminishes with age
Williams, B. J., Bimonte‐Nelson, H. A., & Granholm-Bentley, A.-C. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0477-1 · Cited by 36 · see citing works
Structural determinants of the roles of acetylcholine in cerebral cortex
Descarries, L., Mechawar, N., Aznavour, N., & Watkins, K. C. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)45002-4 · Cited by 36 · see citing works
Modulatory compartments in cortex and local regulation of cholinergic tone
Coppola, J. J., Ward, N. J., Jadi, M. P., & Disney, A. A. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.08.001 · Cited by 35 · see citing works
Muller, J. F., Mascagni, F., Zaric, V., & McDonald, A. J. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23254 · Cited by 34 · see citing works
Structure and function of dual‐source cholinergic modulation in early vision
Krueger, J., & Disney, A. A. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24590 · Cited by 34 · see citing works
Décossas, M., Bloch, B., & Bernard, V. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10734 · Cited by 32 · see citing works
Wester, J. C., & Contreras, D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1644-13.2013 · Cited by 30 · see citing works
Pawlowski, S. A., Gaillard, S., Ghorayeb, I., Ribeiro‐da‐Silva, A., Schlichter, R., & Cordero‐Erausquin, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3954-12.2013 · Cited by 31 · see citing works
Self-citationNicotinic modulation of thalamocortical neurotransmission
Clarke, P. B. S. (2004) · Progress in brain research · doi:10.1016/s0079-6123(03)45017-6 · Cited by 31 · see citing works
Neuronal localization of M2 muscarinic receptor immunoreactivity in the rat amygdala
McDonald, A. J., & Mascagni, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.032 · Cited by 30 · see citing works
Fine structural features of the acetylcholine innervation in the developing neostriatum of rat
Aznavour, N., Mechawar, N., Watkins, K. C., & Descarries, L. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10660 · Cited by 30 · see citing works
Dunant, Y., & Gisiger, V. (2017) · Molecules · doi:10.3390/molecules22081300 · Cited by 28 · see citing works
Mäki-Marttunen, T., & Mäki-Marttunen, V. (2022) · doi:10.1101/2022.03.30.486368 · Cited by 44 · see citing works
Cholinergic and Adenosinergic Modulation of Synaptic Release
Yang, D., Ding, C., Qi, G., & Feldmeyer, D. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2020.06.006 · Cited by 24 · see citing works
Changes with aging in the dopaminergic and noradrenergic innervation of rat neocortex
Allard, S., Gosein, V., Cuello, A. C., & Ribeiro‐da‐Silva, A. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.12.023 · Cited by 24 · see citing works
Self-citationReorganization of the septohippocampal cholinergic fiber system in experimental epilepsy
Soares, J. I., Valente, M. C. A., Andrade, P., Maia, G. H., & Lukoyanov, N. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24235 · Cited by 23 · see citing works
Kanamaru, T., Fujii, H., & Aihara, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053854 · Cited by 23 · see citing works
Endogenous Acetylcholine and Its Modulation of Cortical Microcircuits to Enhance Cognition
Venkatesan, S., Jeoung, H., Chen, T., Power, S. K., Liu, Y., & Lambe, E. K. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_138 · Cited by 21 · see citing works
Griffith, W. H., DuBois, D. W., Fincher, A. S., Peebles, K. A., Bizon, J. L., & Murchison, D. A. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00129.2013 · Cited by 19 · see citing works
Showell, S., Martinez, Y., Gondolfo, S., Boppana, S., & Lawal, H. O. (2020) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2020.103483 · Cited by 18 · see citing works
Structural Organization of Monoamine and Acetylcholine Neuron Systems in the Rat CNS
Descarries, L., & Mechawar, N. (2008) · Springer eBooks · doi:10.1007/978-0-387-30382-6_1 · Cited by 18 · see citing works
Birthelmer, A., Lazaris, A., Schweizer, T., Jackisch, R., & Cassel, J. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00065-0 · Cited by 18 · see citing works
Wang, T., Chen, J., Wang, Y.-J., & Tseng, G. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.025 · Cited by 16 · see citing works
Verhoog, M. B., & Mansvelder, H. D. (2011) · Neural Plasticity · doi:10.1155/2011/870763 · Cited by 16 · see citing works
Altered NGF response but not release in the aged septo-hippocampal cholinergic system
WILLIAMS, B., NELSON, M., Granholm, A., Coultrap, S. J., Browning, M. D., & CURTIS, M. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.07.001 · Cited by 16 · see citing works
Stemmelin, J., Cassel, J., & Kelche, C. R. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1510-9 · Cited by 15 · see citing works
How the Brain Decides what we See
Smythies, J. (2005) · Journal of the Royal Society of Medicine · doi:10.1177/014107680509800106 · Cited by 14 · see citing works
Segovia, G., & Mora, F. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.10.010 · Cited by 14 · see citing works
Qi, G., & Feldmeyer, D. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.843025 · Cited by 10 · see citing works
Aging and subcellular localization of m2 muscarinic autoreceptor in basalocortical neurons in vivo
Décossas, M., Doudnikoff, É., Bloch, B., & Bernard, V. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.09.007 · Cited by 12 · see citing works
White, D., Abreu, R. D. S., Blake, A., Murphy, J., Showell, S., Kitamoto, T., & Lawal, H. O. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104744 · Cited by 11 · see citing works
Csaba, Z., Krejci, É., & Bernard, V. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23268 · Cited by 11 · see citing works
Attention as Sigma-Pi controlled ACh-based feedback
Taylor, J., Hartley, M., & Taylor, N. (2006) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn.2005.1555839 · Cited by 9 · see citing works
The involvement of the cholinergic system in Alzheimer disease
Cuello, A. C. (2025) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19088-9.00005-6 · Cited by 8 · see citing works
Self-citationYamamoto, S., Yamada, J., Ueno, S., Kubota, H., Furukawa, T., Yamamoto, S., & Fukuda, A. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk010 · Cited by 8 · see citing works
- 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 › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review