Two distinct populations of cholinergic neurons in the septum of raccoon (Procyon lotor): Evidence for a separate subset in the lateral septum

Journal of Comparative Neurology

Volumn 412, Issue 1, 1999, Pages 112-122

  Brauer, Kurt ^a   Holzer, Max ^a   Brückner, Gert ^a   Tremere, Liisa ^b   Rasmusson, Douglas D ^b   Poethke, Reinhild ^c   Arendt, Thomas ^a   Härtig, Wolfgang ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b DALHOUSIE UNIVERSITY   (Canada)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Calbindin; Extracellular matrix; Medial septum; Nerve growth factor receptor; Parvalbumin; Wisteria floribunda agglutinin

Indexed keywords

AGGLUTININ; CALBINDIN; CHOLINE ACETYLTRANSFERASE; LECTIN; NEUROTROPHIN RECEPTOR; NITRIC OXIDE SYNTHASE; PARVALBUMIN; PROTEOCHONDROITIN SULFATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMALE; HIPPOCAMPUS; HISTOCHEMISTRY; MALE; NONHUMAN; PERIKARYON; PRIMATE; PRIORITY JOURNAL; RACCOON; RODENT; SEPTUM PELLUCIDUM;

ANIMALS; BRAIN; CELL COUNT; CHOLINE O-ACETYLTRANSFERASE; CHONDROITIN SULFATES; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GAMMA-AMINOBUTYRIC ACID; IMMUNOENZYME TECHNIQUES; LECTINS; MALE; NEURONS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; PARASYMPATHETIC NERVOUS SYSTEM; PARVALBUMINS; PLANT LECTINS; RACCOONS; RECEPTORS, N-ACETYLGLUCOSAMINE;

EID: 0033552061     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990913)412:1<112::AID-CNE8>3.0.CO;2-M     Document Type: Article

References (51)

1. Bigl V, Woolf NJ, Butcher L. 1982. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res Bull 8:727-749.
2. Brauer K, Schober A, Wolff JR, Winkelmann E, Luppa H, Lüth H-J, Böttcher H. 1991. Morphology of neurons in the rat basal forebrain nuclei: comparison of NADPH-diaphorase histochemistry and immunohistochemistry of glutamic acid decarboxylase, choline acetyltransferase, somatostatin and parvalbumin. J Hirnforsch 32:1-17.
3. Brauer K, Härtig W, Bigl V, Brückner G. 1993. Distribution of parvalbumin-containing neurons and lectin-binding perineuronal nets in the rat basal forebrain. Brain Res 631:167-170.
4. Brace G, Wainer BH, Hersh LB. 1985. Immunoaffinity purification of human choline acetyltransferase: comparison of the brain and placental enzymes. J Neurochem 45:611-620.
5. Brückner G, Schober W, Härtig W, Ostermann-Latif C, Webster RW, Dykes DD, Rasmusson DD, Biesold D. 1992. The basal forebrain cholinergic system in the raccoon. J Chem Neuroanat 5:441-452.
6. Bruckner G, Schütz A, Härtig W, Brauer K, Paulke B-R, Bigl V. 1994. Projection of non-cholinergic neurons ensheathed with perineuronal nets to rat mesocortex. J Chem Neuroanat 8:11-18.
7. Brückner G, Härtig W, Kacza J, Seeger J, Welt K, Brauer K. 1996. Extracellular matrix organisation in various regions of the brain gray matter. J Neurocytol 25:333-346.
8. Brückner G, Härtig W, Seeger J, Rübsamen R, Reimer K. Brauer K. 1998. Cortical perineuronal nets in the gray short-tailed opossum (Monodelphis domestica): a distribution pattern contrasting with that shown in placental mammals. Anat Embryol 197:249-262.
9. Celio MR, Baier W, Schärer L, de Viragh PA, Gerday C. 1988. Monoclonal antibodies directed against the calcium-binding protein parvalbumin. Cell Calcium 9:81-86.
10. Celio MR, Baier W, Schärer L, Gregersen HJ, de Viragh PA, Norman AW. 1990. Monoclonal antibodies directed against the calcium binding protein calbindin D-28k. Cell Calcium 11:599-602.
11. Chang H, Kuo H. 1991. Relationship of calbindin D-28k and cholinergic neurons in the nucleus basalis of Meynert of the monkey and the rat. Brain Res 549:141-145.
12. Côté P-Y, Parent A. 1992. Calbindin D-28k and choline acetyltransferase are expressed by different neuronal populations in pedunculopontine nucleus but not in nucleus basalis in squirrel monkeys. Brain Res 593:245-252.
13. Deller T, Leranth C, Frotscher M. 1994. Reciprocal connections of lateral septal neurons and neurons in the lateral hypothalamus in the rat: a combined Phaseolus uulgaris-leucoagglutinin and Fluoro-Gold immunocytochemical study. Neurosci Lett 168:119-122.
14. Freund TF. 1989. GABAergic septohippocampal neurons contain parvalbumin. Brain Res 478:375-381.
15. 28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience 54:461-476.
16. Gritti I, Mainville L, Mancia M, Jones BE. 1997. GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 383:163-177.
17. Härtig W, Brauer K, Brückner G. 1992. Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport 3:869-872.
18. Härtig W, Brauer K, Bigl V, Brückner G. 1994. Chondroitin sulfate proteoglycan-immunoreactivity of lectin-labeled perineuronal nets around parvalbumin-containing neurons. Brain Res 635:307-311.
19. Härtig W, Brückner G, Holzer M, Brauer K, Bigl V. 1995. Digoxigenylated primary antibodies for sensitive dual-peroxidase labelling of neural markers. Histochem Cell Biol 104:467-472.
20. 28k and calretinin in rat and monkey brain. J Neurosci Methods 67:89-95.
21. Hefti F, Hartikka J, Salvaterra WJ, Weinen WJ, Mash D. 1986. Localization of nerve growth factor receptor on cholinergic neurons of the human basal forebrain. Neurosci Lett 69:275-281.
22. Hobohm C, Härtig W, Brauer K, Brückner G. 1998. Low expression of extracellular matrix components in rat brain stem regions containing modulatory aminergic neurons. J Chem Neuroanat 15:135-142.
23. 28k in the monkey medial septal nucleus and nucleus of the diagonal band: an immunocytochemical study. Brain Res 625:328-332.
24. Jakab RL, Leranth C. 1995. Septum. In: Paxinos G, editor. The rat nervous system, 2nd edition. San Diego: Academic Press, p 405-442.
25. D28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:378-396.
26. Kimura H, Tago H, Akiyama H, Hersh LB, Tooyama I, McGeer PL. 1990, Choline acetyltransferase immunopositive neurons in the lateral septum. Brain Res 533:165-170.
27. Kiss J, Patal AJ, Freund TF. 1990. Distribution of septohippocampal neurons containing parvalbumin or choline acetyltransferase in the rat brain. J Comp Neurol 298:362-373.
28. Kitchener PD, Diamond J. 1993. Distribution and colocalization of choline acetyltransferase immunoreactivity and NADPH diaphorase reactivity in neurons within the medial septum and diagonal band of Broca in the rat basal forebrain. J Comp Neurol 335:1-15.
29. Kordower JH, Bartus RT, Bothwell M, Schatteman G, Gash DM. 1988. Nerve growth factor receptor immunoreactivity in the nonhuman primate (Cebus apella): distribution, morphology, and co-localization with cholinergic enzymes. J Comp Neurol 277:465-486.
30. Kosaka T, Heizmann CW, Fujita SC. 1992. Monoclonal antibody 473 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp Brain Res 89:109-114.
31. Leranth C, Frotscher M. 1989. Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J Comp Neurol 289:304-314.
32. Linke R, Frotscher M. 1992. Parvalbumin in the medial septum/diagonal band complex of the African green monkey Cercopithecus aethiops. J Hirnforsch 33:653-660.
33. Maclean CJ, Baker HF, Fine A, Ridley RM. 1997. The distribution of p75 neurotrophin receptor-immunoreactive cells in the forebrain of the common marmoset (Callithrix jacchus). Brain Res Bull 43:197-208.
34. Mesulam M-M, Mufson EJ, Levey AI, Wainer BH. 1983a. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominate), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170-197.
35. Mesulam M-M, Mufson EJ, Wainer BH, Levey AJ. 1983b. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch 1-Ch 6). Neuroscience 10:1185-1201.
36. Mufson EJ, Bothwell M, Hersh LB, Kordower J. 1989. Nerve growth factor receptor profiles in the normal, aged human basal forebrain: colocalization with cholinergic neurons. J Comp Neurol 285:196-217.
37. Oorjitham EG, Godfrey DA, Ross CD, Dunn JD. 1989. Effect of septal ablation on choline acetyltransferase in the paraventricular nucleus. Brain Res Bull 22:277-282.
38. Poethke R, Härtig W, Brückner G, Felgenhauer K, Mäder M. 1997. Characterization of monoclonal and polyclonal antibodies to human choline acetyltransferase and epitope analysis. Biol Chem 378:997-1004.
39. Rasmusson DD. 1982. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J Comp Neurol 205:313-326.
40. Risold PY, Swaneon LW. 1997a. Chemoarchitecture of the rat lateral septal nucleus. Brain Res Rev 24:91-113.
41. Risold PY, Swanson LW. 1997b. Connections of the lateral septal complex. Brain Res Rev 24:115-195.
42. Ross AH, Grob P, Bothwell M, Elder DE, Ernst CS, Marano N, Christ BFD, Slemp CC, Herlyn M, Atkinson B, Koprowski H. 1984. Characterization of nerve growth factor receptor in neural crest tumors using monoclonal antibodies. Proc Natl Acad Sci USA 81:6681-6685.
43. Roßner S, Härtig W, Schliebs R, Brückner G, Brauer K, Perez-Polo JR, Wiley RG, Bigl V. 1995. 192IgG-saporin immunotoxin-induced loss of cholinergic cells differentially activates microglia in rat basal forebrain nuclei. J Neurosci Res 41:335-346.
44. Schober A, Brauer K, Luppa H. 1989. Alternate coexistence of NADPH-diaphorase with choline acetyltransferase or somatostatin in the rat neostriatum and basal forebrain. Acta Histochem Cytochem 22:669-674.
45. Springer JE, Koh S, Tayrien MW, Loy R. 1987. Basal forebrain magnocellular neurons stained for nerve growth factor receptor: correlation with cholinergic cell bodies and effects of axotomy. J Neurosci Res 17:111-118.
46. Staiger JF, Nürnberger F. 1991. The efferent connections of the lateral septal nucleus in the guinea pig: projections to the diencephalon and brainstem. Cell Tissue Res 264:391-413.
47. Swanson LW, Cowan WM. 1979. The connections of the septal region in the rat. J Comp Neurol 186:621-656.
48. NTR. and calbindin-immunoreactivity in cholinergic neurons of the raccoon basal forebrain, Brain Res 797:351-356.
49. Vincent SR, Reiner PR. 1987. The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371-415.
50. Welker WI, Seidenstein S. 1959. Somatic sensory representation in the cerebral cortex of the raccoon (Procyon lotor). J Comp Neurol 111:469-501.
51. Wu C-K, Mesulam M-M, Geula C. 1997. Age-related loss of calbindin from human basal forebrain cholinergic neurons. Neuroreport 8:2209-2213.