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Behavioral neuroanatomy of cholinergic innervation in the primate cerebral cortex

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Central Cholinergic Synaptic Transmission

Part of the book series: Experientia Supplementum ((EXS,volume 57))

Summary

This brief review summarizes the anatomy and behavioral affiliations of cortical cholinergic innervation. A depletion of this innervation has been reported in a number of human neurodegenerative conditions (including Alzheimer’s disease) and may contribute to the genesis of the associated behavioral disturbances.

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References

  • Arendt, T., Bigl, V., Tennstedt, A., and Arendt, A. (1985) Neuronal loss in different parts of the nucleus basalis is related to neuritic plaque formation in cortical target areas in Alzheimer’s disease. J. Neurosci. 14: 1–14.

    Google Scholar 

  • Averback, P . (1981) Lesions of the nucleus ansae peduncularis in neuropsychiatric disease. Arch. Neurol. 38: 230–235

    Google Scholar 

  • Bloxam, C. A., Perry, E. K., Perry, R. H., and Candy, J. M. (1984) neuropathological and neurochemical correlate of Alzheimer-type and Parkinsonian dementia. In: Wurtman, R. J., Corkin, S. H., and Growdon, J. H. (eds), Alzheimer’s Disease: Advances in Basic Research and Therapies. Center for Brain Sciences and Metabolism Charitable Trust, Cambridge, MA, pp. 39–52.

    Google Scholar 

  • Candy, J. M., Perry, R. H., Thompson, J. E., Johnson, M., Oakley, A. E., and Edwardson, J. A. (1985) The current status of the cortical cholinergic system in Alzheimer’s disease and Parkinson’s disease. J. Anat. 140: 309–327.

    Google Scholar 

  • Casanova, M. F., Walker, L. C., Whitehouse, P. J. and Price D. L. (1985) Abnormalities of the nucleus basalis in Down’s Syndrome. Ann. Neurol. 18: 310–313.

    Article  Google Scholar 

  • DeLong, M. R. (1971) Activity of pallidal neurons during movement. J. Neurophysiol. 34: 414–427.

    Google Scholar 

  • Dunnett, S. B., Whishaw, I. Q., Jones, G. H., and Bunch, S. T. (1987) Behavioral, biochemical and histochemical effects of different neurotoxic amino acids injected into nucleus basalis magnocellularis of rats. J. Neurosci. 20: 653–669.

    Article  Google Scholar 

  • Ellison, D. W., Kowall, N. W., and Martin, J. B. (1987) Subset of neurons characterized by the presence of NADPH-diophorase in human substantia innominata. J. comp. Neurol. 260: 233–245.

    Article  Google Scholar 

  • Etienne, P., Robitaille, Y., Wood, P., Gauthier, S., Nair, N. P. V., and Quirion, R. (1986) Nucleus basalis neuronal loss, neuritic plaques and choline acetyltransferase activity in advanced Alzheimer’s disease. J. Neurosci. 19: 1279–1291.

    Article  Google Scholar 

  • Flicker, C., Dean, R. L., Watkins, D. L., Fisher, S. K., and Bartus, R. T. (1983) Behavioral and neurochemical effects following neurotoxic lesions of a major cholinergic input to the cerebral cortex in the rat. Pharmac. Biochem. Behav. 18: 973–981.

    Article  Google Scholar 

  • Gaspar, P., Berger, B., Alvarex, C., Vigny, A., and Henry, J. P., (1985) Catecholaminergic innervation of the septal area in man: Immunocytochemical study using TH and DBH antibodies. J. comp. Neurol. 214: 12–33.

    Article  Google Scholar 

  • German, D. C., Bruce, G., and Hersh, L. B. (1985) Immunohistochemical staining of cholinergic neurons in the human brain using a polyclonal antibody to human choline acetyltransferase. Neurosci. Lett. 61: 1–5.

    Article  Google Scholar 

  • Gorry, J. D. (1963) Studies on the comparative anatomy of the ganglion basale of Meynert. Acta anat. 55: 51–104.

    Article  Google Scholar 

  • Heath, R. G. (1959) Studies in Schizophrenia. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Hefti, F., and Weiner, W. J. (1986) Nerve growth factor and Alzheimer’s disease. Ann. Neurol. 20: 275–281.

    Article  Google Scholar 

  • Iadecola, C., Mraovitch, S., Meeley, M. P., and Reis, D. J. (1983) Lesions of the basal forebrain in rat selectively impair vasodilation elicited from cerebellar fastigial nucleus. Brain Res. 279: 41–52.

    Article  Google Scholar 

  • Johnston, M. V., McKinney, M., and Coyle, J. T. (1979) Evidence for a cholinergic projection to neocortex from neurons in basal forbrain. Proc. natl Acad. Sci. 76: 5392– 5396.

    Google Scholar 

  • Karczmar, A. G. (1975) Cholinergic influences on behavior. In: Waser, P. G. (ed.), Cholinergic Mechanisms. Raven Press, New York, pp. 501–529.

    Google Scholar 

  • Krnjevic, K . (1981) Acetylcholine as a modulator of amino-acid-mediated synaptic transmission. In: The Role of Peptides and Amino Acids as Neurotransmitters. A. Liss, New York, pp. 124–141.

    Google Scholar 

  • McCormick, D. A., and Prince, D. A. (1985) Two types of muscarinic responses to acetylcholine in mammalian cortical neurons. Proc. natl Acad. Sci. USA 82: 6344–6348.

    Article  Google Scholar 

  • Mesulam, M.-M. (1985) Patterns in behavioral neuroanatomy: association areas, the limbic system and hemispheric specialization. In: Mesulam, M.-M. (ed.), Principles of Behavioral Neurology. Contemporary Neurology Series. F. A. Davis Co., Philadelphia, pp. 1–70.

    Google Scholar 

  • Mesulam, M.-M. (1986) Alzheimer’s plaques and cortical cholinergic innervation. Neurosci. 17: 275–276.

    Article  Google Scholar 

  • Mesulam, M.-M. (1987) Asymmetry of neural feedback in the organization of behavioral states. Science 237: 537–538.

    Article  Google Scholar 

  • Mesulam, M.-M., and Geula, C. (1988) Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain. J. comp. Neurol., in press.

    Google Scholar 

  • Mesulam, M.-M., and Mufson, E. J. (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107: 253–274.

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E. J., Levey, A. I., and Wainer, B. H. (1983a) Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey. J. comp. Neurol. 214: 170–197.

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E. J., and Rogers, J. (1987) Age-related shrinkage of cortically projecting cholinergic neurons: A selective effect. Ann. Neurol. 22: 31–36.

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E. J., and Wainer, B. H. (1986a) Three-dimensional representation and cortical projection topography of the nucleus basalis (Ch4) in the macaque: Concurrent demonstration of choline acetyltransferase and retrograde transport with a stabilized tetramethylbenzidine method for HRP. Brain Res. 367: 301–308.

    Article  Google Scholar 

  • Mesulam, M.-M., Mufson, E. J., Wainer, B. H., and Levey, A. I. (1983b) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Chl–Ch6). Neuroscience 10: 1185–1201.

    Article  Google Scholar 

  • Mesulam, M.-M., Rosen, A. D., and Mufson, E. J. (1984) Regional variations in cortical cholinergic innervation: chemoarchitectonics of acetylcholinesterase-containing fibers in the macaque brain. Brain Res. 311: 245–258.

    Article  Google Scholar 

  • Mesulam, M.-M., Volicer, L., Marquis, J. K. Mufson, E. J., and Green, R. C. (1986b) systematic regional differences in the cholinergic innervation of the primate cerebral cortex: Distribution of enzyme activities and some behavioral implications. Ann. Neurol. 19: 144–151.

    Article  Google Scholar 

  • Metherate, R., Tremblay, N., and Dykes, R. W. (1987) Acetylcholine permits long-term enhancement of neuronal responsiveness in cat primary somatosensory cortex. Neuroscience 22: 75–81.

    Article  Google Scholar 

  • Mishkin, M. (1982) A memory system in man and monkey. Phil. Trans. R. Soc. Lond. B 298: 85–92.

    Article  Google Scholar 

  • Mufson, E. J., Kehr, A. D., Wainer, B. H., and Mesulam, M.-M. (1987) Cortical effects of neurotoxic damage to the nucleus basalis in rats: persistent loss of extrinsic cholinergic input and lack of transsynaptic effect upon the number of somatostatin-containing, cholinesterase-positive and cholinergic cortical neurons. Brain Res. 417: 385–388.

    Article  Google Scholar 

  • Mufson, E. J., Martin, T. L., Mash, D. C., Wainer, B. H., and Mesulam, M.-M. (1986) Cholinergic projections from the parabigemenal nucleus (Ch8) to the superior colliculus in the mouse: A combined analysis of HRP transport and choline acetyltransferase immuno- histochemistry. Brain Res. 370: 144–148.

    Article  Google Scholar 

  • Nagai, T., McGeer, P. L., Peng, J. H., McGeer, E. G., and Dolman, C. E. (1983) Choline acetyltransferase immunohistochemistry in brains of Alzheimer’s disease patients and controls. Neurosci. Lett. 36: 195–199.

    Article  Google Scholar 

  • Olds, J., and Milner, P. (1954) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. comp. Physiol. Psychol. 47: 419–427.

    Article  Google Scholar 

  • Orzi, F., Diana, G., Palombo, E., Lenzi, G. L., Bracco, L., and Fieschi, C. (1986) Effects of unilateral lesion of the nucleus basalis on local cerebral glucose utilization in the rat. In: Vezzadini, P., Facchini, A., and Labo, G. (eds), Neuroendocrine System and Aging. Eurage, pp. 259–264.

    Google Scholar 

  • Pearson, R. C. A., Sofroniew, M. V., Cuello, A. C., Powell, T. P. S., Eckenstein, F., Esiri, M. M., and Wilcock G. K. (1984) Persistence of cholinergic neurons in the basal nucleus in a brain with senile demntia of the Alzheimer’s type demonstrated by immunohistochemical staining for choline acetyltransferase. Brain Res. 289: 375–379.

    Article  Google Scholar 

  • Perry, E. K., Tomlinson, B. E., Blessed, G., Bergmann, K., Gibson, P. H., and Perry, R. H. (1978) Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J. 2: 1457–1459.

    Article  Google Scholar 

  • Ramon-Moliner, E., and Nauta, W. J. H. (1966) The isodendritic core of the brain stem. J. comp. Neurol. 126: 311.

    Article  Google Scholar 

  • Ridley, R. M., Murray, T. K., Johnson, J. A., and Baker, H. F. (1986) Learning impairment following lesion of the basal nucleus of Meynert in the marmoset: Modification by cholinergic drugs. Brain Res. 376: 108–116.

    Article  Google Scholar 

  • Rogers, J. D., Brogan, D., and Mirra, S. S. (1985) The nucleus basalis of Meynert in neurological disease: A quantitative morphological study. Ann. Neurol. 17: 163–170.

    Article  Google Scholar 

  • Saper, C. B., and Chelimskyh, T. C. (1984) A cytoarchitectonic and histochemical study of nucleus basalis and associated cell groups in the normal human brain. Neuroscience 13: 1023–1037.

    Article  Google Scholar 

  • Steward, D. J., MacFabe, D. F., and Vanderwolf, C. N. (1984) Cholinergic activation of the electrocorticogram: Role of the substantia innominata and effects of atropine and quinu clidinyl benzylate. Brain Res. 322: 219–232.

    Article  Google Scholar 

  • Szymusiak, R., and McGinty, D. (1986) Sleep suppression following kainic acid-induced lesions of the basal forebrain. Exp. Neurol. 94: 598–614.

    Article  Google Scholar 

  • Tagliavini, F., and Pilleri, G. (1985) Neuronal loss in the basal nucleus of Meynert in a patient with olivopontocerebellar atrophy. Acta neuropath. 66: 127–133.

    Article  Google Scholar 

  • Tago, H., Kimura, H., and Maeda, T. (1986) Visualization of detailed acetylcholinesterase fiber and neuron stainig in rat brain by a sensitive histochemical procedure. J. Histochem. Cytochem. 34: 1431–1438.

    Article  Google Scholar 

  • Vijayashankar, N., and Brody, H. (1979) A quantitative study of the pigmented neurons in the nuclei locus coeruleus and sub coeruleus in man as related to aging. J. Neuropath, exp. Neurol. 38: 490–497

    Article  Google Scholar 

  • Wainer, B. H., Levey, A. I., Mufson, E. J., and Mesulam, M.-M. (1984) Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem. int. 6: 163–182.

    Article  Google Scholar 

  • Woolfe, N. J., and Butcher, L. L. (1981) Cholinergic neurons in the caudate-putamen complex proper are intrinsically organized: A combined Evans Blue and acetylcholinesterase analysis. Brain Res. 7: 487–507.

    Google Scholar 

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© 1989 Birkhäuser Verlag

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Mesulam, MM. (1989). Behavioral neuroanatomy of cholinergic innervation in the primate cerebral cortex. In: Frotscher, M., Misgeld, U. (eds) Central Cholinergic Synaptic Transmission. Experientia Supplementum, vol 57. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-9138-7_1

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  • DOI: https://doi.org/10.1007/978-3-0348-9138-7_1

  • Publisher Name: Birkhäuser Basel

  • Print ISBN: 978-3-0348-9922-2

  • Online ISBN: 978-3-0348-9138-7

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