Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections
Abstract
Cholinergic axons in the human cerebral cortex were analyzed by electron microscopy. Choline acetyltransferase (ChAT) immunoreactivity was used to identify cholinergic axons in samples of anterior temporal lobe removed at surgery. A systematic survey of labeled axon varicosities, visualized in complete serial sections, showed that 67% of all varicosities formed identifiable synaptic specializations. These synapses were usually symmetric and quite small, often present in only one to two serial sections. However, an occasional synapse was asymmetric and larger, seen in five to seven serial sections. The postsynaptic processes at cholinergic synapses were often identified as spiny dendrites or spines. The existence of cholinergic axons in the human cerebral cortex has been demonstrated in numerous studies. Our findings provide the first ultrastructural evidence that these axons make synaptic contact with cortical neurons in the human brain.
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 Smiley et al., 1997
Cites
Hsu, S. M., Raine, L., & Fanger, H. (1981) · Journal of Histochemistry & Cytochemistry · doi:10.1177/29.4.6166661 · Cited by 14,248 · see citing works
The structure of the nervous system of the nematode <i>Caenorhabditis elegans</i>
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · see citing works
The Fine Structure of the Nervous System.
Tennyson, V. M. (1970) · Archives of Neurology · doi:10.1001/archneur.1970.00480240094019 · Cited by 1,946 · see citing works
The Fine Structure of the Nervous System
Afifi, A. K. (1991) · Neurology · doi:10.1212/wnl.41.9.1535-b · Cited by 1,052 · see citing works
Frotscher, M., & Léránth, C. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902390210 · Cited by 600 · 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
Hersch, S. M., Gutekunst, C., Rees, H., Heilman, C. J., & Levey, A. I. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-03351.1994 · Cited by 404 · 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
Hasselmo, M. E., & Bower, J. M. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.5.1222 · Cited by 358 · see citing works
Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice.
Pitler, T. A., & Alger, B. E. (1992) · The Journal of Physiology · doi:10.1113/jphysiol.1992.sp019119 · Cited by 288 · 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
Vidal, C., & Changeux, J. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90558-w · Cited by 240 · 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
Wainer, B. H., Bolam, J. P., Freund, T. F., Henderson, Z., Totterdell, S., & Smith, A. D. (1984) · Brain Research · doi:10.1016/0006-8993(84)90918-1 · Cited by 213 · see citing works
Smiley, J. F., & Goldman-Rakic, P. S. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.3.223 · Cited by 211 · see citing works
Self-citationCholinergic innervation of hippocampal GAD‐ and somatostatin‐immunoreactive commissural neurons
Léránth, C., & Frotscher, M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902610104 · Cited by 189 · see citing works
Frotscher, M., & Léránth, C. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902430106 · Cited by 179 · see citing works
Volume Transmission in the Brain
Weissman, J. D. (1992) · Neurology · doi:10.1212/wnl.42.7.1440-b · Cited by 175 · see citing works
Beaulieu, C., & Somogyi, P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040412 · Cited by 126 · see citing works
Mesulam, M. M., Mufson, E. J., & Wainer, B. H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91607-0 · Cited by 114 · see citing works
Self-citationClarke, D. J. (1985) · Brain Research · doi:10.1016/0006-8993(85)91253-3 · Cited by 112 · see citing works
German, D. C., Bruce, G., & Hersh, L. B. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90391-x · Cited by 103 · 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
Carlsen, J., & Heimer, L. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902440110 · Cited by 84 · see citing works
Synaptic interactions involving acetylcholine, glutamate, and GABA in rat auditory cortex
Metherate, R., & Ashe, J. H. (1995) · Experimental Brain Research · doi:10.1007/bf00228017 · Cited by 78 · see citing works
Aoki, C. J., & Kabak, S. (1992) · Visual Neuroscience · doi:10.1017/s0952523800002832 · Cited by 68 · see citing works
Muscarinic depression of synaptic transmission at the hippocampal mossy fiber synapse
Williams, S., & Johnston, D. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.64.4.1089 · Cited by 61 · see citing works
Regional distribution of neurotrophin receptors in the developing auditory brainstem
Hafidi, A., Moore, T., & Sanes, D. H. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960408)367:3 · Cited by 51 · see citing works
Mesulam, M. M., & Geula, C. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90244-5 · Cited by 44 · see citing works
Self-citationPresynaptic Receptors in the Mammalian Brain
Dunwiddie, T., & Lovinger, D. (1993) · Birkhäuser Boston · doi:10.1007/978-1-4684-6825-0 · Cited by 24 · see citing works
Schwartz, M. L., & Mrzljak, L. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903270105 · Cited by 23 · see citing works
Muscarinic Cholinergic Inhibition of Glutamatergic Transmission
Williams, S. H., & Johnston, D. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-6825-0_3 · Cited by 12 · see citing works
Presynaptic receptors in the mammalian brain
Starke, K. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90363-8 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mesulam, M. (1998) · Brain · doi:10.1093/brain/121.6.1013 · Cited by 3,072 · see citing works
Self-citationAcetylcholine 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
The Cholinergic Lesion of Alzheimer's Disease: Pivotal Factor or Side Show?
Mesulam, M. (2004) · Learning & Memory · doi:10.1101/lm.69204 · Cited by 467 · see citing works
Self-citationCholinergic circuitry of the human nucleus basalis and its fate in Alzheimer's disease
Mesulam, M. M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23415 · Cited by 378 · see citing works
Self-citationPhasic 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 346 · see citing works
The Basal Forebrain Corticopetal System Revisited
Záborszky, L., Pang, K. C. H., Somogyi, J., Nádasdy, Z., & Kalló, I. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09276.x · Cited by 242 · see citing works
Descarries, L., & Mechawar, N. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)25005-x · Cited by 241 · see citing works
The cholinergic innervation of the human cerebral cortex.
Mesulam, M.-M. (2004) · Progress in Brain Research · doi:10.1016/s0079-6123(03)45004-8 · Cited by 211 · see citing works
Self-citationYamasaki, M., Matsui, M., & Watanabe, M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5719-09.2010 · Cited by 203 · see citing works
Muller, J. F., Mascagni, F., & McDonald, A. J. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20832 · Cited by 203 · 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
Non‐synaptic receptors and transporters involved in brain functions and targets of drug treatment
Vizi, E. S., Fekete, Á., Károly, R., & Mike, Á. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00624.x · Cited by 182 · 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
Cholinergic modulation of cognition: Insights from human pharmacological functional neuroimaging
Bentley, P., Driver, J., & Dolan, R. J. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.06.002 · Cited by 173 · see citing works
The Basal Forebrain Cholinergic Projection System in Mice
Záborszky, L., van den Pol, A. N., & Gyengési, E. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10028-7 · Cited by 166 · 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
Postsynaptic targets of somatostatin‐containing interneurons in the rat basolateral amygdala
Muller, J. F., Mascagni, F., & McDonald, A. J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21185 · Cited by 153 · see citing works
Bloem, B., Poorthuis, R. B., & Mansvelder, H. D. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00017 · Cited by 146 · 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
Turrini, P., Casu, M. A., Wong, T. P., De Koninck, Y., Ribeiro-da-Silva, A., & Cuello, A. C. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00172-5 · Cited by 135 · see citing works
Cellular, 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
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
Trueta, C., & De‐Miguel, F. F. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00319 · Cited by 122 · see citing works
Coupled Networks of Parvalbumin-Immunoreactive Interneurons in the Rat Basolateral Amygdala
Muller, J. F., Mascagni, F., & McDonald, A. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0899-05.2005 · Cited by 121 · 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
Disney, A. A., Domakonda, K. V., & Aoki, C. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21096 · Cited by 99 · see citing works
Obermayer, J., Heistek, T. S., Kerkhofs, A., Goriounova, N. A., Kroon, T., Baayen, J. C., Idema, S., Testa-Silva, G., Couey, J. J., & Mansvelder, H. D. (2018) · Nature Communications · doi:10.1038/s41467-018-06628-w · Cited by 102 · see citing works
Obermayer, J., Verhoog, M. B., Luchicchi, A., & Mansvelder, H. D. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00100 · Cited by 98 · see citing works
Layer-specific cholinergic control of human and mouse cortical synaptic plasticity
Verhoog, M. B., Obermayer, J., Kortleven, C., Wilbers, R., Wester, J., Baayen, J. C., de Kock, C. P. J., Meredith, R. M., & Mansvelder, H. D. (2016) · Nature Communications · doi:10.1038/ncomms12826 · Cited by 95 · see citing works
Muller, J. F., Mascagni, F., & McDonald, A. J. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21486 · Cited by 93 · see citing works
Dopaminergic innervation of interneurons in the rat basolateral amygdala
Pinard, C. R., Muller, J. F., Mascagni, F., & McDonald, A. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.09.043 · Cited by 75 · see citing works
Rapid Neuromodulation of Layer 1 Interneurons in Human Neocortex
Poorthuis, R. B., Muhammad, K., Wang, M., Verhoog, M. B., Junek, S., Wrana, A., Mansvelder, H. D., & Letzkus, J. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.111 · Cited by 70 · see citing works
Fuxé, K., Borroto‐Escuela, D. O., Romero‐Fernandez, W., Dı́az-Cabiale, Z., Rivera, A., Ferraro, L., Tanganelli, S., Tarakanov, A. O., Garriga, P., Narváez, J. Á., et al. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00136 · Cited by 73 · see citing works
Volume Transmission in the Brain: Beyond the Synapse
Taber, K. H., & Hurley, R. A. (2014) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.13110351 · Cited by 70 · 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
Ikonomović, M. D., Abrahamson, E. E., Isanski, B. A., Wuu, J., Mufson, E. J., & DeKosky, S. T. (2007) · Archives of Neurology · doi:10.1001/archneur.64.9.1312 · 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
Dopaminergic innervation of pyramidal cells in the rat basolateral amygdala
Muller, J. F., Mascagni, F., & McDonald, A. J. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0196-y · Cited by 61 · see citing works
Smiley, J. F., & Mesulam, M. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00202-4 · Cited by 60 · see citing works
Self-citationThe hypothesis of an ambient level of acetylcholine in the central nervous system
Descarries, L. (1998) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(98)80013-2 · 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
Hay, Y. A., Lambolez, B., & Tricoire, L. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv085 · Cited by 52 · see citing works
Localisation of pre- and postsynaptic cholinergic markers in the human brain
Wevers, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.025 · 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
Muller, J. F., Mascagni, F., & McDonald, A. J. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22550 · Cited by 49 · see citing works
Postsynaptic targets of GABAergic basal forebrain projections to the basolateral amygdala
McDonald, A. J., Muller, J. F., & Mascagni, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.027 · Cited by 48 · see citing works
Cholinergic Circuits and Signaling in the Pathophysiology of Schizophrenia
Berman, J. A., Talmage, D. A., & Role, L. W. (2007) · International Review of Neurobiology · doi:10.1016/s0074-7742(06)78007-2 · Cited by 47 · see citing works
Cholinergic and serotonergic modulation of visual information processing in monkey V1
Shimegi, S., Kimura, A., Sato, A., Aoyama, C., Mizuyama, R., Tsunoda, K., Ueda, F., Araki, S., Goya, R., & Sato, H. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.09.001 · Cited by 40 · see citing works
Giuliano, 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
Cholinergic Mechanisms in the Cerebral Cortex
Ovsepian, S. V., O’Leary, V. B., & Záborszky, L. (2015) · The Neuroscientist · doi:10.1177/1073858415588264 · Cited by 40 · see citing works
Anisuzzaman, 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
Organization of the Basal Forebrain Cholinergic Projection System
Záborszky, L., Duque, A., Gielow, M. R., Gombkötő, P., Nádasdy, Z., & Somogyi, J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00019-x · Cited by 38 · see citing works
Krenz, I., Kalkan, D., Wevers, A., de Vos, R. A. I., Steur, E. N. H. J., Lindstrom, J. M., Pilz, K., Nowacki, S., Schütz, U., Moser, N., et al. (2001) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(01)00112-0 · Cited by 37 · 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
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
Wester, J. C., & Contreras, D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1644-13.2013 · Cited by 30 · see citing works
Hernández‐Pérez, O. R., Hernández, V. S., Nava-Kopp, A. T., Barrio, R. A., Seifi, M., Swinny, J. D., Eiden, L. E., & Zhang, L. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00196 · Cited by 30 · 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
Muller, J. F., Mascagni, F., Zaric, V., Mott, D. D., & McDonald, A. J. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.23959 · Cited by 21 · see citing works
Bautista, T. G., Sun, Q., Zhao, W., & Pilowsky, P. M. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22495 · Cited by 18 · see citing works
Ovsepian, S. V., & Herms, J. W. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.05.005 · 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
Verhoog, M. B., & Mansvelder, H. D. (2011) · Neural Plasticity · doi:10.1155/2011/870763 · Cited by 16 · see citing works
Eid, L., Parent, A., & Parent, M. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0960-0 · Cited by 16 · see citing works
Vijayraghavan, S., & Everling, S. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.648624 · Cited by 15 · 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
Asynaptic and Synaptic Innervation by Acetylcholine Neurons of the Central Nervous System
Descarries, L., & Parent, M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418675-0.00014-6 · Cited by 6 · see citing works
The micro-structure of attention
Taylor, N. R., Hartley, M., & Taylor, J. G. (2006) · Neural Networks · doi:10.1016/j.neunet.2006.08.002 · Cited by 6 · see citing works
Pinard, C. R., Mascagni, F., Muller, J. F., & McDonald, A. J. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.062 · Cited by 4 · see citing works
Kwapiszewski, J. T., Rivera-Pérez, L. M., & Roberts, M. T. (2023) · Journal of the Association for Research in Otolaryngology · doi:10.1007/s10162-022-00885-9 · Cited by 4 · see citing works
Cholinergic modulation of cortical activity
Steriade, M., & Descarries, L. (2006) · CRC Press eBooks · doi:10.1201/b14486-16 · Cited by 3 · see citing works
Garzón, M., Chan, J., Mackie, K., & Pickel, V. M. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac024 · Cited by 2 · see citing works
Coward, L. A. (2013) · Springer eBooks · doi:10.1007/978-94-007-7107-9_5
Lee, K. S., Sahlender, D. A., Blanc, J., Jorstad, A., Gasselin, C., Clerc-Rosset, S., Markopoulos, F., Petersen, C. C. H., Holtmaat, A. J. D. G., & Knott, G. W. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.11.744243
- Authors
- Smiley, J. F., Morrell, F., & Mesulam, M. M.
- Affiliations
- Northwestern University (US)
- Rush University Medical Center (US)
- Venue
- Experimental Neurology
- Publisher
- Elsevier BV
- Published
- 1997-04
- Volume
- 144
- Issue
- 2
- Pages
- 361-368
- ISSN
- 0014-4886 (ISSN-L)
- OpenAlex
- W2075240805
- Cited by
- 79
- References
- 34
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 3 · 2017: 1 · 2016: 4 · 2015: 2 · 2014: 9 · 2013: 8 · 2012: 4
- FWCI
- 0.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Experimental Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ns020285-15)
- National Institute of Neurological Disorders and Stroke (NS 20285)
- 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 synapses, cholinergic axons, human cerebral cortex, choline acetyltransferase, synaptic ultrastructure, axonal varicosities, postsynaptic spines, anterior temporal lobe
- MeSH terms
- Adult, Cerebral Cortex, Child, Choline O-Acetyltransferase, Cholinergic Fibers, Female, Humans, Male, Microscopy, Electron, Microtomy, Nerve Tissue Proteins, Synapses, Temporal Lobe, Biomarkers
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
