The distribution and morphological characteristics of cholinergic cells in the brain of monotremes as revealed by ChAT immunohistochemistry

Brain, Behavior and Evolution

Volumn 60, Issue 5, 2002, Pages 275-297

  Manger, Paul R ^a,c   Fahringer, Heidi M ^a   Pettigrew, John D ^b   Siegel, Jerome M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

Acetylcholine; Choline acetyltransferase; Echidna; Mammals; Monotremes; Platypus; Sleep

Indexed keywords

CHOLINE ACETYLTRANSFERASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL AGGREGATION; CELL NUCLEUS; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CORPUS STRIATUM; CRANIAL NERVE; ECHIDNA; FOREBRAIN; HABENULA; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; MONOTREMATE; NONHUMAN; PHENOMENOLOGY; PLATYPUS; PRIORITY JOURNAL; SLEEP; SPINAL CORD;

ANIMALS; BRAIN; BRAIN MAPPING; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; ECHIDNA; EVOLUTION; HYPOTHALAMUS; IMMUNOENZYME TECHNIQUES; NEURONS; PHYLOGENY; PLATYPUS; SLEEP;

EUTHERIA; HIATUS; MAMMALIA; MONOTREMATA; ORNITHORHYNCHUS ANATINUS; TACHYGLOSSUS ACULEATUS; TETRAPODA;

EID: 0036904199     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000067195     Document Type: Article

References (68)

1. Abbie, A.A. (1934) The brainstem and cerebellum of Echidna aculeata. Philos. Trans. R. Soc. Lond. B,224:1-74.
2. Allison, T., H. Van Twyver, and W.R. Goff (1972) Electrophysiological studies of the echidna,Tachyglossus aculeatus. I. Waking and sleep. Arch. Ital. Biol.,110:145-184.
3. Armstrong, D.M., C.B. Saper, A.I. Levey, B.H. Wainer, and R.D. Terry (1983) Distribution of cholinergic neurons in rat brain: Demonstrated by the immunocytochemical localization of choline acetyltransferase. J. Comp. Neurol., 216:53-68.
4. Bartus, R.T., R.L. Dean, B. Beer, and A.S. Lippa (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science,217:408-417.
5. Brantley, R.K., and A.H. Bass (1988) Cholinergic neurons in the brain of a teleost fish(Porichthys notatus)located with a monoclonal antibody to choline acetyltransferase. J. Comp. Neurol., 275:87-105.
6. 15O PET study. Brain, 120: 1173-1197.
7. Brauth, S.E., C.A. Kitt, D.L. Price, and B.H. Wain-er (1985) Cholinergic neurons in the telencephalon of the reptile Caiman crocodilus. Neurosci. Lett.,58:235-240.
8. Butler, A.B., and W. Hodos (1996) Comparative Vertebrate Neuroanatomy. Evolution and Adaptation. Wiley-Liss, New York.
9. Ekström, P. (1987) Distribution of choline acetyltransferase-immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.). J. Comp. Neurol.,256:494-515.
10. Everitt, B.J., T.E. Sirkia, A.C. Roberts, G.H. Jones, and T.W. Robbins (1988) Distribution and some projections of cholinergic neurons in the brain of the common marmoset, Callithrix jacchus. J. Comp. Neurol.,271:533-558.
11. Frank, M.G., and H.C. Heller (1997) Development of REM and slow wave sleep in the rat. Am. J. Physiol.,272:R1792-R1799.
12. Gallyas, F. (1979) Silver staining of myelin by means of physical development. Neurol. Res., 1: 203-209.
13. Garcia-Rill, E., C.R. Houser, R.D. Skinner, W. Smith, and D.J. Woodward (1987) Locomotion-inducing sites in the vicinity of the pedun-culopontine nucleus. Brain Res. Bull.,18:731-738.
14. Griffiths, M. (1978) The Biology of the Monotremes. Academic Press, New York.
15. Grigg, G.C., M.L. Augee, and L.A. Beard (1992) Thermal relations of free-living echidnas during activity and hibernation in a cold climate. In Platypus and Echidnas (ed. by M.L. Augee), R. Zool. Soc. NSW, Sydney, Australia, pp. 160-173.
16. Hines, M. (1929) The brain of Ornithorhynchus anatinus. Philos. Trans. R. Soc. Lond. B,217: 155-287.
17. Hoogland, P.V., and E. Vermeulen-VanderZee (1990) Distribution of choline acetyltransferase immunoreactivity in the telencephalon of the lizard Gekko gecko. Brain Behav. Evol.,36: 378-390.
18. Jones, E.G. (1985) The Thalamus. Plenum Press, New York.
19. Jones, B.E., and A. Beaudet (1987) Distribution of acetylcholine and catecholamine neurons in the cat brainstem: A choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J. Comp. Neurol.,261:15-32.
20. Jouvet, M. (1962) Recherches sur les structures nerveuses et les mechanismes responsables des differentes phases du sommeil physiologique. Arch. Ital. Biol.,100:125-206.
21. Kelland, M.D., and D. Asdourian (1989) Pendunculopontine tegmental nucleus-induced inhibition of muscle activity in the rat. Behav. Brain Res.,34:213-234.
22. Kimura, H., P.L. McGreer, J.H. Peng, and E.G. McGreer (1981) The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J. Comp. Neurol., 200:151-201.
23. Kirsch, J.A.W., and G.C. Mayer (1998) The platypus is not a rodent: DNA hybridisation, amniote phylogeny, and the palimpsest theory. Philos. Trans. R. Soc. Lond. B, 353: 1221-1237.
24. Krubitzer, L.A., P.R. Manger, J.D. Pettigrew, and M.B. Calford (1995) The organization of somatosensory cortex in monotremes: In search of the prototypical plan. J. Comp. Neurol.,351: 261-306.
25. Manger, P.R., H.M. Fahringer, J.D. Pettigrew, and J.M. Siegel (2002a) The distribution and morphological characteristics of catecholaminergic cells in the brain of monotremes as revealed by tyrosine hydroxylase immunohistochemistry. Brain Behav. Evol.,60:298-314.
26. Manger, P.R., H.M. Fahringer, J.D. Pettigrew, and J.M. Siegel (2002b) The distribution and morphological characteristics of serotonergic cells in the brain of monotremes. Brain Behav. Evol.,60:315-332.
27. Marin, O., W.J.A.J. Smeets, and A. González (1997) Distribution of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles waltl) amphibians. J. Comp. Neurol.,382:499-534.
28. Mason, W.T., Y.W. Ho, F. Eckenstein, and G.I. Hatton (1983) Mapping of cholinergic neurons associated with rat supraoptic nucleus: Combined immunocytochemical and histochemical identification. Brain Res. Bull.,11:617-626.
29. McGinty, D.J. (1969) Somnolence, recovery and hyposomnia following ventro-medial diencephalic lesions in the rat. Electroenceph. Clin. Neurophysiol.,26:70-79.
30. McGinty, D.J., M. Stevenson, T. Hoppenbrouwers, R.M Harper, M.B. Sterman, and J. Hodgman (1977) Polygraphic studies of kitten development: Sleep state patterns. Dev. Psychobiol., 10:455-469.
31. Medina, L., and A. Reiner (1994) Distribution of choline acetyltransferase activity in the pigeon brain. J. Comp. Neurol.,340:1-41.
32. Medina, L., W.J.A.J. Smeets, P.V. Hoogland, and L. Puelles (1993) Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti. J. Comp. Neurol., 331:261-285.
33. Mesulam, M.M., E.J. Mufson, A.I. Levey, and B.H. Wainer (1984) Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience, 12:669-686.
34. Mesulam, M.M., C. Geula, M.A. Bothwell, and L.B. Hersh (1989) Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons. J. Comp. Neurol., 281: 611-633.
35. Mizukawa, K., P.L. McGeer, H. Tago, J.H. Peng, E.G. McGeer, and H. Kimura (1986) The cho-linergic system of the human hindbrain studied by choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Brain Res.,379:39-55.
36. Molist, P., S. Maslam, E. Velzing, and B.L. Roberts (1993) The organization of cholinergic neurons in the mesencephalon of the eel, Anguilla anguilla, as determined by choline acetyltransferase immunohistochemistry and acetylcholinesterase enzyme histochemistry. Cell Tissue Res., 271:555-566.
37. Mufson, E.J., P.H. Desan, M.M. Mesulam, B.H. Wainer, and A.I. Levey (1984) Choline acetyltransferase-like immunoreactivity in the forebrain of the red-eared pond turtle (Pseudemys scripta elegans). Brain Res.,323:103-108.
38. Musser, A.M., and M. Archer (1998) New information about the skull and dentary of the Miocene platypus Obdurodon dicksoni and a discussion of ornithorhynchid relationships. Philos. Trans. R. Soc. Lond. B,353:1063-1079.
39. Nicol, S.C., N.A. Andersen, N.H. Phillips, and R.J. Berger (2000) The echidna manifests typical characters of rapid eye movement sleep. Neurosci. Lett.,283:49-52.
40. Palkovits, M., and D.M. Jacobowitz (1974) Topographic atlas of catecholamine and acetylcholinesterase-containing neurons in the rat brain. II. Hindbrain (mesencephalon, rhombencephalon). J. Comp. Neurol.,157:29-42.
41. Parnavelas, J.G., W. Kelly, E. Franke, and F. Eckenstein (1986) Cholinergic neurons and fibers in the rat visual cortex. J. Neurocytol.,15: 329-336.
42. Pirlot, P., and J. Nelson (1978) Volumetric analyses of monotreme brains. In Monotreme Biology (ed. by M.L. Augee), R. Zool. Soc. NSW, Sydney, Australia, pp. 171-180.
43. Powers, A.S., and A. Reiner (1993) The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav. Evol.,41: 326-345.
44. Puelles, L. (1995) A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav. Evol.,46:319-337.
45. Reiner, A. (1991) A comparison of neurotransmitter-specific and neuropeptide-specific neuronal cell types present in the dorsal cortex in turtles with those present in the isocortex in mammals: Implications for the evolution of isocortex. Brain Behav. Evol.,38:53-91.
46. Reiner, P.B., and S.R. Vincent (1987) Topographic relations of cholinergic and noradrenergic neurons in the feline pontomesencephalic tegmentum: An immunohistochemical study. Brain Res. Bull.,19:705-714.
47. Satoh, K., and H.C. Fibiger (1985a) Distribution of central cholinergic neurons in the baboon (Papio papio). I. General morphology. J. Comp. Neurol.,236:197-214.
48. Satoh, K., and H.C. Fibiger (1985b) Distribution of central cholinergic neurons in the baboon (Papio papio). II. A topographic atlas correlated with catecholamine neurons. J. Comp. Neurol., 236:215-233.
49. Satoh, K., D.M. Armstrong, and H.C. Fibiger (1983) A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry. Brain Res. Bull.,11:693-720.
50. Shiromani, P.J., D.M. Armstrong, A. Berkowitz, D.V. Jeste, and J.C. Gillin (1988) Distribution of choline acetyltransferase immunoreactive somata in the feline brainstem: Implications for REM sleep generation. Sleep,11:1-16.
51. Shoham, S., and P. Teitelbaum (1982) Subcortical waking and sleep during lateral hypothalamic 'somnolence' in rats. Physiol. Behav.,28:323-333.
52. Siegel, J.M. (2000) Brainstem mechanisms generating REM sleep. In Principals and Practice of Sleep Medicine 2nd Ed. (ed. by M.K. Kryger, T. Roth and W.C. Dement), Saunders, New York, pp. 112-133.
53. Siegel, J.M. (1999) The evolution of REM sleep. In Handbook of Behavioral State Control (ed. by R. Lydic and C. Baghdoyan), CRC Press, Boca Raton, FL, pp. 87-100.
54. Siegel, J.M., P.R. Manger, R. Nienhuis, H.M. Fahringer, and J.D. Pettigrew (1996) The echidna Tachyglossus aculeatus combines REM and non-REM aspects in a single sleep state: Implications for the evolution of sleep. J. Neurosci., 16:3500-3506.
55. Siegel, J.M., P.R. Manger, R. Nienhuis, H.M. Fahringer, and J.D. Pettigrew (1998) Monotremes and the evolution of rapid eye movement sleep. Philos. Trans. R. Soc. Lond. B, 353: 1147-1157.
56. Siegel, J.M., P.R. Manger, R. Nienhuis, H.M. Fahringer, and J.D. Pettigrew (1999) Sleep in the platypus. Neuroscience,9:391-400.
57. Smith, G. (1988) Animal models of Alzheimer's disease: experimental cholinergic denervation. Brain Res. Rev.,13:103-118.
58. Sofroniew, M.V., P.E. Campbell, A.C. Cuello, and F. Eckenstein (1985) Central cholinergic neurons visualized by immunohistochemical detection of choline acetyltransferase. In The Rat Nervous System Vol. 1, Forebrain and Midbrain (ed. by G. Paxinos), Academic Press, New York, pp. 471-485.
59. Steriade, M., D.A. McCormick, and T.J. Sejnowski (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science,262:679-685.
60. Stewart, D., D.F. Macfabe, and C.H. Vanderwolf (1984) Cholinergic activation of the substantia innominata and effects of atropine and quinucavinyl benzilate. Brain Res.,322:219-232.
61. Szymusiak, R., J. Danowski, and D. McGinty (1994) REM sleep-suppressing effects of atropine in cats vary with environmental temperature. Brain Res.,636:115-118.
62. Tago, H., P.L. McGeer, G. Bruce, and L.B. Hersh (1987) Distribution of choline acetyltransferase-containing neurons of the hypothalamus. Brain Res.,415:49-62.
63. Tago, H., P.L. McGeer, E.G. McGeer, H. Akiyama, and L.B. Hersh (1989) Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res.,495:271-297.
64. Vanderwolf, C.H. (1987) Near-total loss of 'learning' and 'memory' as a result of combined cholinergic and serotonergic blockade in the rat. Behav. Brain Res.,23:43-57.
65. Webster, H.H., and B.E. Jones (1988) Neurotoxic lesions of the dorsolateral pontomesencephalic tegmentum-cholinergic cell area in the cat. II. Effects upon sleep-waking states. Brain Res., 458:285-302.
66. Woolf, N.J. (1991) Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol., 37:475-524.
67. Woolf, N.J., and L.L. Butcher (1986) Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res. Bull.,16:603-637.
68. Woolf, N.J., and L.L. Butcher (1989) Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res. Bull.,23:519-540.