Nuclear organization of cholinergic, putative catecholaminergic, serotonergic and orexinergic systems in the brain of the African pygmy mouse (Mus minutoides): Organizational complexity is preserved in small brains

Journal of Chemical Neuroanatomy

Volumn 44, Issue 1, 2012, Pages 45-56

  Kruger, Jean Leigh ^a   Patzke, Nina ^a   Fuxe, Kjell ^b   Bennett, Nigel C ^c   Manger, Paul R ^a  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Choline acetyl transferase; Evolution; Hypocretin; Mammal; Rodent; Serotonin; Tyrosine hydroxylase

Indexed keywords

CHOLINERGIC RECEPTOR; SEROTONIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BRAIN SIZE; CATECHOLAMINE NERVE CELL; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CRANIAL NERVE; DIENCEPHALON; EVOLUTION; FOREBRAIN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; LOCUS CERULEUS; MALE; MEDULLA OBLONGATA; MESENCEPHALON; MOUSE; MUS MINUTOIDES; NERVE CELL NETWORK; NEUROANATOMY; NONHUMAN; OLFACTORY BULB; OREXINERGIC SYSTEM; PONS; PRIORITY JOURNAL; PUTATIVE CATECHOLAMINERGIC SYSTEM; RHOMBENCEPHALON; SEROTONINERGIC SYSTEM;

ACETYLCHOLINE; ANIMALS; BASAL GANGLIA; BRAIN; CATECHOLAMINES; CELL NUCLEUS; CEREBRAL CORTEX; CORPUS STRIATUM; DIENCEPHALON; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEDULLA OBLONGATA; MESENCEPHALON; MICE; NEUROPEPTIDES; RHOMBENCEPHALON; SEROTONIN;

EID: 84861481723     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2012.04.002     Document Type: Article

References (79)

1. Agnati L.F., Franzen O., Ferre S., Leo G., Franco R., Fuxe K. Possible role of intramembrane receptor-receptor interactions in memory and learning via formation of long-lived heteromeric complexes: focus on motor learning in the basal ganglia. Journal of Neural Transmission Supplementum 2003, 65:1-28.
2. Baldo B.A., Daniel R.A., Berridge C.W., Kelley A.E. Overlapping distributions of orexin/hypocretin- and dopamine-beta-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. Journal of Comparative Neurology 2003, 464:220-237.
3. Bayraktar T., Staiger J.F., Acsady L., Cozzari C., Freund T.F., Zilles K. Co-localization of vasoactive intestinal polypeptide, gamma-aminobutyric acid and choline acetyltransferase in the neocortical interneurons of the adult rat. Brain Research 1997, 757:209-217.
4. Bhagwandin A., Fuxe K., Manger P.R. Choline acetyltransferase immunoreactive cortical interneurons do not occur in all rodents: a study of the phylogenetic occurrence of this neural characteristic. Journal of Chemical Neuroanatomy 2006, 32:208-216.
5. Bhagwandin A., Fuxe K., Bennett N.C., Manger P.R. Nuclear organization and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brains of two species of African mole-rat. Journal of Chemical Neuroanatomy 2008, 35:371-387.
6. Bhagwandin A., Fuxe K., Bennett N.C., Manger P.R. Distribution of orexinergic neurons and their terminal networks in the brains of two species of African mole rats. Journal of Chemical Neuroanatomy 2011, 41:32-42.
7. Björklund A., Lindvall O. Dopamine-containing systems in the CNS. Handbook of Chemical Neuroanatomy 1984, Vol. 2. Classical Neurotransmitters in the CNS, Part 1:55-122. Elsevier, Amsterdam.
8. Blanga-Kanfi S., Miranda H., Penn O., Pupko T., DeBry R.W., Huchon D. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evolutionary Biology 2009, 9:71.
9. Chen C.T., Dun S.L., Kwok E.H., Dun N.J., Chang J.K. Orexin A-like immunoreactivity in the rat brain. Neuroscience Letters 1999, 260:161-164.
10. Crutcher K.A., Humbertson A.O. The organization of monoamine neurons within the brainstem of the North American opossum (Didelphis virginiana). J. Comp. Neurol. 1978, 179:195-222.
11. Cutler D.J., Morris R., Sheridhar V., Wattam T.A.K., Kolmes S., Patel S., Atch J.R.S., Wilson S., Buckingham R.E., Evans M.L., Leslie R.A., Williams G. Differential distribution of orexin-A and orexin-b immunoreactivity in the rat brain and spinal cord. Peptides 1999, 20:1455-1470.
12. Da Silva J.N., Fuxe K., Manger P.R. Nuclear parcellation of certain immunohistochemically identifiable neuronal systems in the midbrain and pons of the Highveld mole-rat (Cryptomys hottentotus). Journal of Chemical Neuroanatomy 2006, 31:37-50.
13. Dahlström A., Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamine in the cell bodies of brainstem neurons. Acta Physiologica Scandinavica 1964, 62:1-52.
14. Dell L.-A., Kruger J.-L., Bhagwandin A., Jillani N.E., Pettigrew J.D., Manger P.R. Nuclear organization of cholinergic, putative catecholaminergic and serotonergic systems in the brains of two megachiropteran species. Journal of Chemical Neuroanatomy 2010, 40:177-195.
15. Downs C.T., Perrin M.R. The thermal biology of southern Africa's smallest rodent, Mus minutoides. South African Journal of Science 1996, 92:282-285.
16. Dwarika S., Maseko B.C., Ihunwo A.O., Fuxe K., Manger P.R. Distribution and morphology of putative catecholaminergic and serotonergic neurons in the brain of the greater canerat, Thryonomys swinderianus. Journal of Chemical Neuroanatomy 2008, 35:108-122.
17. Ebbesson S.O. The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity. Cell and Tissue Research 1980, 213:179-212.
18. Eckenstein F., Baughman R.W. Two types of cholinergic innervation in the cortex, one co-localised with vasoactive intestinal polypeptide. Nature 1984, 309:153-155.
19. Espana R.A., Reis K.M., Valentino R.J., Berridge C.W. Organization of hypocretin/orexin efferents to locus coeruleus and basal forebrain arousal-related structures. Journal of Comparative Neurology 2005, 481:160-178.
20. Feldman J.L., Ellenberger H.H. Central coordination of respiratory and cardiovascular control in mammals. Annual Review of Physiology 1988, 50:593-606.
21. Ferguson A.V., Samson W.K. The orexin/hypocretin system: a critical regulator of neuroendocrine and autonomic function. Frontiers in Neuroendocrinology 2003, 24:141-150.
22. Ferreira G., Meurisse M., Tillet Y., Levy F. Distribution and co-localization of choline acetyltransferase and P75 neurotrophin receptors in the sheep basal forebrain: implications for the use of a specific cholinergic immunotoxin. Neuroscience 2001, 104:419-439.
23. Fuxe K. Cellular localization of monoamines in the median eminence and the infundibular stem of some mammals. Zeitschrift für Zellforschung 1964, 61:710-724.
24. Fuxe K., Hökfelt T., Ungerstedt U. Distribution of monoamines in the mammalian central nervous system by histochemical studies. Metabolism of Amines in the Brain 1969, 10-22. Macmillan, London. G. Hooper (Ed.).
25. Fuxe K., Hökfelt T., Ungerstedt U. Morphological and functional aspects of central monoamine neurons. International Review of Neurobiology 1970, 13:93-126.
26. Fuxe K., Härfstrand A., Agnati L.F., Kalia M., Fredholm B., Svensson T., Gustafsson J.A., Lang R., Ganten D. Central catecholamine-neuropeptide Y interactions at the pre- and postsynaptic level in cardiovascular centers. Journal of Cardiovascular Pharmacology 1987, 10(Suppl. 12):S1-S13.
27. Gallyas F. Silver staining of myelin by means of physical development. Neurological Research 1979, 1:203-209.
28. Ginovart N., Marcel D., Bezin L., Garcia C., Gagne C., Pujol J.F., Weissman D. Tyrosine hydroxylase expression within Balb/C and C57Black6 mouse locus coeruleus. I. Topological organization and phenotypic plasticity of the enzyme-containing cell population. Brain Research 1996, 721:11-21.
29. Gravett N., Bhagwandin A., Fuxe K., Manger P.R. Distribution of orexin-A immunoreactive neurons and their terminal networks in the brain of the rock hyrax, Procavia capensis. Journal of Chemical Neuroanatomy 2011, 41:86-96.
30. Hökfelt T., Johansson O., Fuxe K., Goldstein M., Park D. Immunohistochemical studies on the localization and distribution of monoamine neuron systems in the rat brain. I. Tyrosine hydroxylase in the mes- and diencephalon. Medical Biology 1976, 54:427-453.
31. Hökfelt T., Martenson R., Björklund A., Kleinau S., Goldstein M. Distributional maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. Handbook of Chemical Neuroanatomy 1984, Vol. 2. Classical Neurotransmitters in the CNS, Part 1:277-379. Elsevier, Amsterdam.
32. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiological Reviews 1992, 72:165-229.
33. Jansa S.A., Weksler M. Phylogeny of the murid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Molecular Phylogenetics and Evolution 2004, 31:256-276.
34. Jones B.E., Cuello A.C. Afferents to the basal forebrain cholinergic cell area from pontomesencephalic catecholamine, serotonin and acetylcholine neurons. Neuroscience 1989, 31:37-61.
35. Kerley G.I.H. Seed removal by rodents, birds and ants in the semiarid Karoo, South Africa. Journal of Arid Environment 1991, 20:63-69.
36. Khorooshi R.M., Klingenspor M. Neuronal distribution of melanin-concentrating hormone, cocaine- and amphetamine regulated transcript and orexin B in the brain of the Djungarian hamster (Phodopus sungorus). Journal of Chemical Neuroanatomy 2005, 29:137-148.
37. Kirouac G.J., Parson M.P., Li S. Orexin (hypocretin) innervation of the paraventricular nucleus of the thalamus. Brain Research 2005, 1059:179-188.
38. Kitahama K., Geffard M., Okamura H., Nagatsu I., Mons N., Jouvet M. Dopamine- and dopa-immunoreactive neurons in the cat forebrain with reference to tyrosine hydroxylase-immunohistochemistry. Brain Research 1990, 518:83-94.
39. Kitahama K., Sakamoto N., Jouvet A., Nagatsu I., Pearson J. Dopamine-beta-hydroxylase and tyrosine hydroxylase immunoreactive neurons in the human brainstem. Journal of Chemical Neuroanatomy 1996, 10:137-146.
40. Kruger J.-L., Dell L.-A., Pettigrew J.D., Manger P.R. Cellular location and major terminal networks of the orexinergic system in the brains of five microchiropteran species. Journal of Chemical Neuroanatomy 2010, 40:256-262.
41. Kruger J.-L., Dell L.-A., Bhagwandin A., Jillani N.E., Pettigrew J.D., Manger P.R. Nuclear organization of cholinergic, putative catecholaminergic and serotonergic systems in the brains of five microchiropteran species. Journal of Chemical Neuroanatomy 2010, 40:210-222.
42. Leshin L.S., Kraeling R.R., Kineman R.D., Barb C.R., Rampacek G.B. Immunocytochemical distribution of catecholamine-synthesizing neurons in the hypothalamus and pituitary gland of pigs: tyrosine hydroxylase and dopamine-β-hydroxylase. Journal of Comparative Neurology 1995, 364:151-168.
43. Limacher A.M., Bhagwandin A., Fuxe K., Manger P.R. Nuclear organization and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brain of the Cape porcupine (Hystrix africaeaustralis): increased brain size does not lead to increased organizational complexity. Journal of Chemical Neuroanatomy 2008, 36:33-52.
44. Manger P.R. Establishing order at the systems level in mammalian brain evolution. Brain Research Bulletin 2005, 66:282-289.
45. Manger P.R., Fahringer H.M., Pettigrew J.D., Siegel J.M. Distribution and morphology of cholinergic neurons in the brain of the monotremes as revealed by ChAT immunohistochemistry. Brain Behav. Evol. 2002, 60:275-297.
46. Manger P.R., Fahringer H.M., Pettigrew J.D., Siegel J.M. Distribution and morphology of serotonergic neurons in the brain of the monotremes. Brain Behav. Evol. 2002, 60:315-332.
47. Manger P.R., Cort J., Ebrahim N., Goodman A., Henning J., Karolia M., Rodrigues S.L., Strkalj G. Is 21st century neuroscience too focussed on the rat/mouse model of brain function and dysfunction?. Frontiers in Neuroanatomy 2008, 2:5.
48. Maseko B.C., Bourne J.A., Manger P.R. Distribution and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brain of the Egyptian Rousette flying fox, Rousettus aegyptiacus. Journal of Chemical Neuroanatomy 2007, 34:108-127.
49. McGranaghan P.A., Piggins H.D. Orexin A-like immunoreactivity in the hypothalamus and thalamus of the Syrian hamster (Mesocricetus auratus) and Siberain hamster (Phodopus sungorus), with special reference to circadian structures. Brain Research 2001, 904:234-244.
50. Meister B., Hökfelt T., Steinbusch H.W., Skagerberg G., Lindvall O., Geffard M., Joh T.H., Cuello A.C., Goldstein M. Do tyrosine hydroxylase-immunoreactive neurons in the ventrolateral arcuate nucleus produce dopamine or only L-dopa?. Journal of Chemical Neuroanatomy 1988, 1:59-64.
51. Mintz E.M., van Den Pol A.N., Casano A.A., Albers H.E. Distribution of hypocretin (orexin) immunoreactivity in the central nervous system of Syrian hamsters (Mesocricetus auratus). Journal of Chemical Neuroanatomy 2001, 21:225-238.
52. Monadjem A. Populations dynamics of Mus minutoides and Steatomys pratensis (Muridae: Rodentia) in a subtropical grassland in Swaziland. African Journal of Ecology 1999, 37:202-210.
53. Moon D.J., Maseko B.C., Ihunwo A., Fuxe K., Manger P.R. Distribution and morphology of catecholaminergic and serotonergic neurons in the brain of the highveld gerbil, Tatera brantsii. Journal of Chemical Neuroanatomy 2007, 34:134-144.
54. Nixon J.P., Smale L. A comparative analysis of the distribution of immunoreactive orexin A and B in the brain of nocturnal and diurnal rodents. Behavioral and Brain Functions 2007, 3:28.
55. Novak C.M., Albers H.E. Localization of hypocretin-like immunoreactivity in the brain of the diurnal rodent, Arvicanthis niloticus. Journal of Chemical Neuroanatomy 2002, 23:49-58.
56. Olson L., Fuxe K. Further mapping out of the central noradrenaline neurons systems: projections of the subcoeruleus area. Brain Research 1972, 43:289-295.
57. Paxinos G., Watson C. Chemoarchitectonic Atlas of the Mouse Brain 2009, Academic Press, New York.
58. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., Kilduff T.S. Neurons containing hypocretin (orexin) project to multiple neuronal systems. Journal of Neuroscience 1998, 18:9996-10015.
59. Previc F.H. Dopamine and the origins of human intelligence. Brain and Cognition 1999, 41:299-350.
60. Reiner P.B., Fibiger H.C. Functional heterogeneity of central cholinergic systems. Psychopharmacology: The Fourth Generation of Progress 1995, 147-153. Raven, New York. F.E. Bloom, D.J. Kupfer (Eds.).
61. Rodrigues S.L., Maseko B.C., Ihunwo A.O., Fuxe K., Manger P.R. Nuclear organization and morphology of serotonergic neurons in the brain of the Nile crocodile, Crocodylus niloticus. Journal of Chemical Neuroanatomy 2008, 35:133-145.
62. Ruggiero D.A., Anwar M., Gootman P.M. Presumptive adrenergic neurons containing phenylethanolamine N-methyltransferase immunoreactivity in the medulla oblongata of neonatal swine. Brain Research 1992, 583:105-119.
63. Siegel J.M. The stuff dreams are made of: anatomical substrates of REM sleep. Nature Neuroscience 2006, 9:721-722.
64. Skagerberg G., Meister B., Hökfelt T., Lindvall O., Goldstein M., Joh T., Cuello A.C. Studies on dopamine-, tyrosine hydroxylase- and aromatic L-amino acid decarboxylase-containing cells in the rat diencephalon: comparison between formaldehyde-induced histofluorescence and immunofluorescence. Neuroscience 1988, 24:605-620.
65. Smeets W.J.A.J., González A. Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Research Reviews 2000, 33:308-379.
66. Steinbusch H.W.M. Distribution of serotonin-immunoreactivity in the central nervous system of the rat - cell bodies and terminals. Neuroscience 1981, 6:557-618.
67. Stephan H., Frahm H., Baron G. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatologica 1981, 35:1-29.
68. Takakusaki K., Takahashi K., Saitoh K., Harada H., Okumura T., Kayama Y., Koyama Y. Orexinergic projections to the cat midbrain mediate alternation of emotional behavioural states from locomotion to cataplexy. Journal of Physiology 2005, 568:1003-1020.
69. Tillet Y., Kitahama K. Distribution of central catecholaminergic neurons: a comparison between ungulates, humans and other species. Histology and Histopathology 1998, 13:1163-1177.
70. Törk I. Anatomy of the serotonergic system. Annals of the New York Academy of Sciences 1990, 600:9-35.
71. Veyrunes F., Catalan J., Tatard C., Cellier-Holzem E., Watson J., Chevret P., Robinson T.J., Britton-Davidian J. Mitochondrial and chromosomal insights into karyotypic evolution of the pygmy mouse, Mus minutoides, in South Africa. Chromosome Research 2010, 18:563-574.
72. Vidal L., Blanchard J., Morin L.P. Hypothalamic and zona incerta neurons expressing hypocretin, but not melanin concentrating hormone, project to the hamster intergeniculate leaflet. Neuroscience 2005, 134:1081-1090.
73. von Coelln R., Thomas B., Savitt J.M., Lim K.L., Sasaki M., Hess E.J., Dawson V.L., Dawson T.M. Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proceedings of the National Academy of Sciences of United States of America 2004, 101:10744-10749.
74. Wagner D., Salin-Pascual R., Greco M.A., Shiromani P.J. Distribution of hypocretin-containing neurons in the lateral hypothalamus and c-fos-immunoreactive neurons in the VLPO. Sleep Research Online 2000, 3:35-42.
75. Weihe E., Depboylu C., Schultz B., Schafer M.K.H., Edien L.E. Three types of tyrosine hydroxylase-positive CNS neurons distinguished by Dopa decarboxylase and VMAT2 co-expression. Cellular and Molecular Neurobiology 2006, 26:659-678.
76. Wilson D.E., Reeder D.M. Mammal Species of the World: A Taxonomic and Geographic Reference 2005, Johns Hopkins University Press, Baltimore, USA.
77. Woolf N.J. Cholinergic systems in mammalian brain and spinal cord. Progress in Neurobiology 1991, 37:475-524.
78. Woolf N.J., Hameroff S.R. A quantum approach to visual consciousness. Trends in Cognitive Sciences 2001, 5:472-748.
79. Zeitzer J.M., Buckmaster C.L., Parker K.J., Hauck C.M., Lyons D.M., Mignot E. Circadian and homeostatic regulation of hypocretin in a primate model: implications for the consolidation of wakefulness. Journal of Neuroscience 2003, 23:3555-3560.