Cholinergic innervation of the monkey amygdala: An immunohistochemical analysis with antisera to choline acetyltransferase

Journal of Comparative Neurology - Tập 281 Số 3 - Trang 337-361 - 1989
David G. Amaral1, Julia L. Bassett1
1The Salk Institute for Biological Studies, La Jolla, California 92037

Tóm tắt

AbstractThe organization of the cholinergic innervation of the macaque monkey amygdaloid complex was investigated by means of immunohistochemical techniques and either a polyclonal antiserum or a monoclonal antibody directed against the specific synthetic enzyme choline acetyltransferase (ChAT). Adjacent series of sections were processed histochemically for the demonstration of the degradative enzyme acetylcholinesterase (AChE) or for cell bodies with thionin. The density of ChAT immunoreactivity differed substantially among the various nuclei and cortical regions of the amygdala. In general, the distribution of ChAT immunoreactivity paralleled the pattern of AChE staining. One notable exception was the presence of AChE containing cell bodies in addition to AChE positive fibers within nearly all of the nuclear and cortical regions. In contrast, ChAT immunoreactivity was associated only with fibers and terminals.The highest density of ChAT immunoreactive fibers and terminals was consistently observed in the magnocellular subdivision of the basal nucleus. Staining was substantially less dense in the more ventrally situated parvicellular subdivision. Medially, in the adjacent accessory basal nucleus, immunoreactive fibers and terminals were densest in the magnocellular and superficial subdivisions and least prominent in the parvicellular subdivision. Of the deep nuclei, the lateral nucleus generally contained the least ChAT immunoreactive terminals and processes. Only its more densely cellular ventrolateral portion contained appreciable fiber and terminal staining.One of the more distinctive patterns of ChAT immunoreactivity was seen in the nucleus of the lateral olfactory tract. Here, ChAT positive fibers formed pericellular basket plexuses around unstained cell bodies. This unique pattern of staining was used to delineate the boundaries of the nucleus and indicated that it is present for much of the rostrocaudal extent of the amygdala. Another region of conspicuous staining on the medial surface of the amygdala was the sulcal portion of the periamygdaloid cortex. This region, associated with the sulcus semiannularis and bordering the entorhinal cortex, consistently contained dense immunoreactivity. The central nucleus also presented a somewhat idiosyncratic pattern of ChAT staining. The lateral subdivision had a diffuse distribution of immunoreactivity in which focal patches of more densely stained terminals and occasional fine fibers were embedded. In contrast, the medial subdivision contained a larger number of thicker, stained fibers without diffuse background labeling. Of the remaining amygdaloid nuclei, the amygdalohippocampal area contained dense ChAT staining, whereas progressively lighter staining was seen in anterior amygdaloid, posterior cortical, anterior cortical, and medial nuclei.

Từ khóa


Tài liệu tham khảo

10.1007/BF00247288

10.1002/cne.902300402

10.1016/0006-8993(82)90974-X

10.1126/science.7046051

Ben‐Ari Y., 1981, The Amygdaloid Complex, 163

10.1016/0006-8993(75)90786-6

10.1016/0006-8993(77)90397-3

Butcher L. L., 1984, Handbook of Chemical Neuroanatomy, 1

10.1002/cne.902340203

10.1016/S0140-6736(76)91936-X

10.1126/science.6140757

10.1001/archneur.1974.00490320001001

10.1523/JNEUROSCI.03-11-02286.1983

10.1002/j.1460-2075.1982.tb01175.x

10.1016/0306-4522(81)90065-8

Fallon J. H., 1981, The Amygdaloid Complex, 175

10.1016/0165-0173(82)90011-X

10.1002/ana.410190305

Gaffan D., 1987, Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys, J. Neuroscience, 7, 2285

10.1007/BF00325634

10.1002/cne.901290107

10.1159/000145181

10.1016/0196-9781(83)90015-3

10.1016/0006-8993(84)90386-X

10.1007/BF00335536

10.1016/0306-4522(86)90297-6

10.1177/33.2.2578498

Hellendal R. P., 1986, The distribution of choline acetyltransferase in the rat amygdaloid complex and adjacent cortical areas, as determined by quantitative micro‐assay and immunocytochemistry, J. Comp. Neurol., 249, 486, 10.1002/cne.902490405

10.1001/archneur.1980.00500590049006

10.1016/0006-8993(78)90408-0

10.1523/JNEUROSCI.06-01-00281.1986

Kaada B., 1972, The Neurobiology of the AmygdalaB, 145

Kemper T. L., 1983, Banbury Report 15. Biological Aspects of Alzheimer's Disease, 31

10.1002/cne.902000202

10.1016/0006-8993(87)90783-9

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

10.1016/0024-3205(79)90596-4

10.1016/0306-4522(83)90042-8

10.1523/JNEUROSCI.03-01-00001.1983

10.1016/0304-3940(85)90186-7

10.1002/cne.901900407

10.1002/cne.902140206

10.1016/0306-4522(83)90108-2

10.1016/0306-4522(84)90064-2

10.1098/rstb.1982.0074

10.1126/science.3983648

Nagai T., 1982, Cholinergic projections from the basal forebrain of rat to the amygdala, J. Neurosci., 2, 513, 10.1523/JNEUROSCI.02-04-00513.1982

10.1016/0304-3940(85)90422-7

Nakamura Y., 1976, Regional distribution of choline acetyltransferase and acetylcholinesterase activity in baboon brain. Folia Psychiatr, Neurol. Jpn., 30, 185

Nitecka L., 1971, Acetylcholinesterase activity in the nuclei of the amygdaloid complex in the rat, Acta Neurobiol. Exp., 31, 383

10.1002/cne.901940113

Ottersen O. P., 1981, The Amygdaloid Complex, 91

Ottersen O. P., 1986, Excitatory Amino Acids and Epilepsy, 53, 10.1007/978-1-4684-7971-3_4

Parent A., 1971, Comparative histochemical study of the amygdaloid complex, J. Hirnforsch., 13, 90

Perry E. K. R. H. Perry B. E.Tomlinson andP. H.Gibson(1980) Coenzyme a‐acetylating enzymes in Alzheimer's disease: Possible cholinergic “compartment” of pyruvate dehydrogenase.Neurosci. Lett.105–110.

Price J. L., 1987, Handbook of Chemical Neuroanatomy, 279

10.1016/0306-4522(82)90156-7

10.1016/0304-3940(82)90155-0

10.1002/cne.902420102

Shiosaka S., 1983, Chemical Neuroanatomy, 359

Silver A., 1974, The Biology of Cholinesterases

Storandt M. J. Botwinick andW. L.Danziger(1985)Longitudinal Changes: Mild SDAT and Matched Healthy Controls. In L. W. Poon (ed): Handbook for the Clinical Memory Assessment of Older Adults.

Svendson C. N., 1985, Acetylcholinesterase staining of the human amygdala, Neurosci. Lett., 54, 313, 10.1016/S0304-3940(85)80097-5

10.1002/cne.902270406

10.1016/0361-9230(87)90015-3

10.1016/0197-0186(84)90089-5

Wang S‐C., 1980, Distribution of acetylcholinesterase in the limbic system of the brain of the rabbit, Acta Anat., 108, 175, 10.1159/000145298

Whitehouse P. J., 1985, An in vitro receptor autoradiographic study of muscarinic cholinergic receptor subtypes in the amygdala and neocortex of patients with Alzheimer's disease, Neurology., 1, 217

10.1016/0361-9230(84)90236-3

10.1016/0304-3940(86)90032-7

10.1007/BF00489974

Zimmer J., 1983, Neurobiology of the Hippocampus, 39