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

Journal of Comparative Neurology - Tập 214 Số 2 - Trang 170-197 - 1983
M.‐Marsel Mesulam1, Elliott J. Mufson1, Allan I. Levey2, Bruce H. Wainer2
1Bullard and Denny-Brown Lclboratories and Behavioral Neurology Section, Harvard Neurology Department and Charles A. Dana Research Institute, Beth Israel Hospital, Boston, Massachusetts 02215
2Departments of Pathology and Pediatrics and Joseph P. Kennedy Jr. Mental Retardation Research Center, University of Chicago, Chicago, Illinois 60637

Tóm tắt

Abstract

The organization of projections from the cholinergic neurons of the basal forebrain to neocortex and associated structures was investigated in the rhesus monkey with the help of horseradish peroxidase transport, acetyl‐cholinesterase histochemistry, and choline acetyltransferase immunohis‐tochemistry. Four groups of neurons contained cholinergic perikarya and were designated as Chl‐Ch4. The Ch1 group corresponds to the medial septal nucleus; about 10% of its neurons are cholinergic, and it provides a substantial projection to the hippocampus. The Ch2 group corresponds to the vertical nucleus of the diagonal band; at least 70% of its neurons are cholinergic, and it is the major source of innervation that the hippocampus and hypothalamus receive from the Chl‐Ch4 complex. The Ch3 group most closely corresponds to the horizontal nucleus of the diagonal band; only 1% of its neurons can definitely be shown to be cholinergic, and it is the major source of Chl‐Ch4 projections to the olfactory bulb. The Ch4 group most closely corresponds to the nucleus basalis of Meynert; at least 90% of its neurons are cholinergic, and it has projections to widespread areas of cortex and to the amygdala. In fact, the Ch4 group provides the single major source of cholinergic innervation for the entire cortical surface. In this respect, it is analogous to the raphe nuclei and to the nucleus locus coeruleus, which constitute the major sources of widespread cortical serotonergic and nor‐adrenergic innervation, respectively.

The extensive Ch4 group can be divided into several subdivisions. Each subdivision has a preferential set of targets for its projections even though the connection patterns contain considerable overlap. The anteromedial subdivision of Ch4 is the major source of cholinergic projections to areas on the medial aspect of the cerebral hemispheres; the anterolateral Ch4 sub‐division is the major source of cholinergic projections to frontoparietal op‐ercular areas and to the amygdala; the intermediate Ch4 subdivision pro‐vides the major cholinergic input for a variety of dorsal prefrontal, insular, posterior parietal, inferotemporal, and peristriate areas; and the posterior subdivision of Ch4 provides the major cholinergic innervation of superior temporal and immediately adjacent areas.

The basal forebrain in the human contains a cytoarchitechture analogous to that of the monkey. The Ch4 group (nucleus basalis) of the human is very extensive and can be subdivided into the same components that were identfied in the monkey brain. Pathological changes in Ch4 neurons have been described in a variety of human disease. In Alzheimer's disease, the relatively selective depression of neocortical cholinergic innervation may be closely associated with the neuronal loss in Ch4, which has also been described inthis condition.

In the rhesus monkey, all types of cortical areas receive substantial projections from the hippocampus. Virtually all of this hypothalamic input into neocortex arises from acetylcholinesterase‐rich neurons which lack choline acetyltransferase. The hypothalamocortical pathway is therefore acetylcholinesterase‐rich but not cholinergic.

Từ khóa


Tài liệu tham khảo

10.1002/cne.901890402

10.1001/archneur.1981.00510040056009

Beccari N., 1943, Neurologia Comparata Anatomo‐Funzionale Dei Ver‐tebrati Compresso L'Uomo

10.1016/0361-9230(82)90101-0

10.1016/0006-8993(80)90434-5

Bloom F. E., 1964, Analysis of individual rabbit olfactory bulb neuron responses to the microelectrophoresis of acetylcholine, norepinephrine and serotonin synergists and antago‐nists, J. Pharmacol. Exp. Ther., 146, 16

Burton M. J., 1975, Visual and taste neurons in the lateral hypothnlamus and substantia innominata: Modulation of responsiveness by hunger, J. Physiol. (Lond.), 252, 50

10.1097/00005053-195212000-00019

10.1002/cne.901910304

Crosby E. G., 1962, Correlative Anatomy of the Nervous System

10.1007/BF00496691

10.1007/BF00528020

Davics P., 1976, Selective loss of central cholinergic neurons in Alzheimer's disease, Lancet, 2, 1403

10.1152/jn.1971.34.3.414

Divae I., 1975, Magnocellular nuclei of the basal forebrain project to neo‐cortex, brain stem, and olfactory bulb. Review of some functional cor‐relates, Brain Res., 93, 385, 10.1016/0006-8993(75)90178-X

10.1001/archneur.1974.00490320001001

Dudar J. D., 1975, The effect of septal nuclei stimulation on the release of acetylcholine from the rabbit hippocampus, Brain Res., 83, 133, 10.1016/0006-8993(75)90863-X

Enimcrs R., 1963, A Stereotaxic Atlas of the Brain of the Squirrel Monkey (Saimiri sciureus)

10.1016/0306-4522(79)90215-X

10.1016/0006-8993(79)90559-6

Foix C., 1925, Anatomie Cerebrale Noyaux Gris Cen‐traux et Region Mesencephalo‐Sous‐Optique

Friedcmann M., 1911, Die Cytoarchitektonikdes Zwischenhirns der Cer‐copithekcn mit besonderer Berucksichtigung des Thalamus opticus, J. Psychol. Neurol. (Leipzig), 18, 309

10.1007/BF00325634

10.1159/000142464

10.1126/science.142.3590.409

Heimer L., 1975, Golgi Centennial Symposium Proceedings, 177

Henderson Z., 1981, A projection from acetylcholinesterase‐containing neurons in the diagonal band to the occipital cortex of the rat, Neu‐roscience, 6, 1081

Hilt D. C., 1982, Pick Disease: Loss of neurons in the nucleus basalis, Neurology, 32, A229

10.1007/BF00686763

10.1002/cne.901570103

10.1073/pnas.76.10.5392

10.1007/BF00237760

10.1002/cne.901670402

Karczmar A. G., 1975, Cholinergic Mechanisms, 501

10.1016/0014-4886(78)90263-7

10.1126/science.1114317

10.1126/science.6990490

10.1002/cne.902000202

10.1016/0006-8993(78)91047-8

Kodama S., 1929, Pathologisch‐anatomische Untersuchungen mit Bezug auf die sorgenannten Basalganglien und ihre Adnexe. Neurologische und Psychiatrische Abhandlungen aus dem Schweize, Archiv fur Neu‐rologie und Psychiatrie, 8, 1

Kolliker A., 1896, Nervensystem

10.1113/jphysiol.1963.sp007106

10.1113/jphysiol.1963.sp007107

Krnjevic K., 1965, A histochemical study of cholinergic fibers in the cerebral cortex, J. Anat., 99, 711

10.1016/0006-8993(74)90806-3

10.1111/j.1471-4159.1973.tb12157.x

10.1016/0006-8993(76)90399-1

10.1016/0306-4522(80)90195-5

10.1016/0014-4886(77)90238-2

Levey A. I. D. M.Armstrong S. F.Atwoh R. D.Terry andB. H.Wainer(1983a) Monoclonal antibodies to choline acetyltransferasc: Production specificity and immunohistochemistry.J. Neurosci.(in press).

Levey A. I., 1982, Immunochcmical studies of bovine and Inimnn choline‐o‐acetyltrnnsferase using monoclonal an‐UlniilliiH, .J. Nmmiulliilll., 39, 1652

Levey A. I. B. H.Wainer E. J.Mufson andM.‐M.Mesulam(1983b) Co‐localization of acetylcholinesterase and choline acefyltransferase in the rat cerebrum.Neuroscience. (in press).

Levvy F. H., 1914, Zur pathologischen Anatomie der Paralysis agitans, Dcutsh. Z. Nervenhoilk., 50, 50

McLennan H., 1978, Pharmacological characterization of the excitatory cholinergic receptors of rat central neurons, Neuro‐pharmacology, 17, 329

10.1002/cne.902030311

Mellgrcn S. I., 1973, Changes in acetylcholinesterase and distribution of degenerating fibers in the hippocampal region after septal lesions in the rat, Brain Res., 52, 19, 10.1016/0006-8993(73)90648-3

10.1177/24.12.63512

10.1177/24.12.826585

10.1177/26.2.24068

Mesulam M.‐M., 1982, Tracing Neural Connections with Horseradish Peroxidase, 1

McSuliun M. M., 1982, Insula of the old world monkey. I. Architectonics in the insulo‐orbito‐temporal component of the par‐alimbic brain, J. Comp. Neurol., 212, 1, 10.1002/cne.902120102

10.1016/0006-8993(76)90385-1

Mesulam M.‐M., 1977, Substantia innominata, septal area and nuclei of the diagonal band in the rhesus monkey: Organization of efferents and their acetylcholinesterase his‐tochemistry, Soc. Neurosci. Abstr., 3, 202

Meynert T., 1872, A Manual of Histology, 650

Mufson E. J., 1982, Cholinergic projections from the mesencephalic tegmentum to neocortex in rhesus monkey, Soc. Neurosci. Abstr., 8, 135

Nauta W. J. H., 1969, The Hypothalamus, 136

Papez J. W., 1934, Thalamic nuclei of pith ecus (macacus) rhesus I. Ventral thalamus, Arch. Neurol. Psychiatr., 32, 1, 10.1001/archneurpsyc.1934.02250070007001

10.1016/0006-8993(81)90415-7

Parent A., 1979, Advances in Neurology, 1

10.1016/0022-510X(77)90036-3

Pcpeu G., 1971, Brain acetylcholine levels in rats with septal lesions, Life Sci., 10, 181, 10.1016/0024-3205(71)90246-3

10.1159/000128232

10.1016/0022-510X(77)90105-8

Price J. L., 1981, An autoradiographic study of the pro‐jections of the central nucleus of the monkey amygdala, J. Neurosci., 1, 1242, 10.1523/JNEUROSCI.01-11-01242.1981

Price J. L., 1970, An experimental study of the origin and course of the centrifugal fibers to the olfactory bulb in the rat, J. Anat., 107, 215

10.1002/cne.901260301

Reichert C. B., 1861, Der Bau Des Menschlichen Gthirns

10.1016/0014-4886(82)90173-X

Roberts T. S., 1963, Insular and opercular cortex and its thalamic projection in Macaca mulatta, Schweitz. Arch. Neurol. Neu‐rochir. Psychiatr., 92, 1

Rosene D. L., 1978, Centrifugal efferents to the olfactory bulb in the rhesus monkey, Soc. Neurosci. Abstr., 4, 91

10.1177/26.1.413864

10.1016/0304-3940(82)90155-0

10.1016/0006-8993(82)90615-1

10.1002/cne.901840202

Shute C. C. D., 1970, The Hypothal‐amus, 167

Stephan H., 1964, Cytoarchitectonics of the septal nuclei in the old world monkeys (Cercopithecus and Colobus), J. Hirnforsch., 7, 1

Sternberger L. A., 1979, Immunohistochemistry, 104

10.1126/science.175440

10.1523/JNEUROSCI.01-07-00784.1981

10.1016/0361-9230(78)90032-1

10.1002/cne.900730106

10.1016/0006-8993(80)91089-6

10.1016/0165-0173(80)90011-9

10.1002/ana.410100203

10.1016/0361-9230(82)90102-2