Orexinergic bouton density is lower in the cerebral cortex of cetaceans compared to artiodactyls

Journal of Chemical Neuroanatomy

Volumn 68, Issue , 2015, Pages 61-76

  Dell, Leigh Anne ^a   Spocter, Muhammad A ^a,b   Patzke, Nina ^a   Karlson, Karl Æ ^c   Alagaili, Abdulaziz N ^d,e   Bennett, Nigel C ^d,f   Muhammed, Osama B ^d   Bertelsen, Mads F ^g   Siegel, Jerome M ^h   Manger, Paul R ^a,d  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^b DES MOINES UNIVERSITY   (United States)

^c REYKJAVIK UNIVERSITY   (Iceland)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

^e Saudi Wildlife Authority   (Saudi Arabia)

^f UNIVERSITY OF PRETORIA   (South Africa)

^g CENTER FOR ZOO AND WILD ANIMAL HEALTH   (Denmark)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cetartiodactyla; Comparative neuroanatomy; Comparative sleep; Evolution; Hypocretin; Mammalia; Orexin

Indexed keywords

NEUROPEPTIDE; OREXIN;

ANIMAL TISSUE; ANTERIOR CINGULATE; AROUSAL; ARTICLE; ARTIODACTYLA; BRAIN; BRAIN CORTEX; CETARTIODACTYLA; COMPARATIVE STUDY; GLIA CELL; IMMUNOHISTOCHEMISTRY; INNERVATION; NERVE CELL; NERVE FIBER; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; SPECIES; STAINING; STEREOMETRY; ANATOMY AND HISTOLOGY; ANIMAL; CELL COUNT; CELL SIZE; CETACEA; CYTOLOGY; EVOLUTION; GLIA; METABOLISM; NERVE ENDING; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; ARTIODACTYLA; BIOLOGICAL EVOLUTION; CELL COUNT; CELL SIZE; CEREBRAL CORTEX; CETACEA; IMMUNOHISTOCHEMISTRY; NEUROGLIA; NEURONS; OREXINS; PRESYNAPTIC TERMINALS;

EID: 84941552585     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2015.07.007     Document Type: Article

References (65)

1. Alexandre C., Andermann M.L., Scammell T.E. Control of arousal by the orexin neurons. Curr. Opin. Neurobiol. 2013, 23:752-759.
2. Badlangana N.L., Adams J.W., Manger P.R. The giraffe (Giraffa camelopardalis) cervical vertebral column: a heuristic example in understanding evolutionary processes. Zool. J. Linn. Soc. 2009, 155:736-757.
3. Bayer L., Serafin M., Eggermann E., Saint-Mleux B., Machard D., Jones B.E., Muhlethaler M. Exclusive postsynaptic action of hypocretin-orexin on sublayer 6b cortical neurons. J. Neurosci. 2004, 24:6760-6764.
4. Bell F.R., Itabisashi T. The electroencephalogram of sheep and goats with special reference to rumination. Physiol. Behav. 1973, 11:503-514.
5. 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. J. Chem. Neuroanat. 2011, 41:32-42.
6. Bhagwandin A., Gravett N., Hemingway J., Oosthuizen M.K., Bennett N.C., Siegel J.M., Manger P.R. Orexinergic neuron numbers in three species of African mole rats with rhythmic and arrhythmic chronotypes. Neuroscience 2011, 199:153-165.
7. Blouin A.M., Fried I., Wilson C.L., Staba R.J., Behnke E.J., Lam H.A., Maidment N.T., Karlsson K.Æ., Lapierre J.L., Siegel J.M. Human hypocretin and melanin-concentrating hormone levels are linked to emotion and social interaction. Nat. Commun. 2013, 4:1547.
8. Branstetter B.K., Finneran J.J., Flethcer E.A., Weisman B.C., Ridgway S.H. Dolphins can maintain vigilant behavior through echolocation for 15 days with interruption or cognitive impairment. PLoS ONE 2012, 7:e47478.
9. Calvey T., Patzke N., Kaswera C., Gilissen E., Bennett N.C., Manger P.R. Nuclear organization of some immunohistochemically identifiable neural systems in three Afrotherian species - Potomogale velox, Amblysomus hottentotus and Petrodromus tetradactylus. J. Chem. Neuroanat. 2013, 50-51:48-65.
10. Datta S., MacLean R.R. Neurobiological mechanisms for the regulation of mammalian sleep-wake behavior: reinterpretation of historical evidence and inclusion of contemporary cellular and molecular evidence. Neurosci. Biobehav. Rev. 2007, 31:775-824.
11. Del Cid-Pellitero E., Garzón M. Hypocretin1/orexin-A immunoreactive axons form few synaptic contacts on rat ventral tegmental area neurons that project to the medial prefrontal cortex. BMC Neurosci. 2011, 7(15):105.
12. Dell L.A., Patzke N., Bhagwandin A., Bux F., Fuxe K., Barber G., Siegel J.M., Manger P.R. Organization and number of orexinergic neurons in the hypothalamus of two species of Cetartiodactyla: a comparison of giraffe (Giraffa camelopardalis) and harbour porpoise (Phocoena phocoena). J. Chem. Neuroanat. 2012, 44:98-109.
13. Dell L.A., Kruger J.L., Pettigrew J.D., Manger P.R. Cellular location and major terminal networks of the orexinergic system in the brain of two megachiropterans. J. Chem. Neuroanat. 2013, 53:64-71.
14. Edwards C.M., Abusnana S., Sunter D., Murphy K.G., Ghatei M.A., Bloom S.R. The effect of the orexins on food intake: comparison with neuropeptide Y, melanin-concentrating hormone and galanin. J. Endocrinol. 1999, 160:R7-R12.
15. Ettrup K.S., Srensen J.S., Bjarkam C.R. The anatomy of the Göttingen minipig hypothalamus. J. Chem. Neuroanat. 2010, 39:151-165.
16. Fadel J., Frederick-Duus D. Orexin/hypocretin modulation of the basal forebrain cholinergic system: insights from in vivo microdialysis studies. Pharmacol. Biochem. Behav. 2008, 90:156-162.
17. Fuxe K., Dahlstrom A.B., Jonsson G., Marcellino D., Guescini M., Dam M., Manger P., Agnati L. The discovery of central monoamine neurons gave volume transmission to the wired brain. Prog. Neurobiol. 2010, 90:82-100.
18. 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. J. Chem. Neuroanat. 2011, 41:86-96.
19. Gundersen H.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Moller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 1988, 96:857-881.
20. Gundersen H.J., Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 1987, 147:229-263.
21. Hofle N., Paus T., Reutens D., Fiset P., Gotman J., Evans A.C., Jones B.E. Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J. Neurosci. 1997, 17:4800-4808.
22. Horvath T.L., Peyron C., Diano S., Ivanov A., Aston-Jones G., Kilduff T.S., van den Pol A.N. Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J. Comp. Neurol. 1999, 415:145-159.
23. Iqbal J., Pompolo S., Sakurai T., Clarke I.J. Evidence that orexin-containing neurons provide direct input to gonadotrophin-releasing hormone neurones in the ovine hypothalamus. J. Neuroendocrinol. 2001, 13:1033-1041.
24. Jessen C. Brain cooling: an economy mode of temperature regulation in artiodactyls. News Physiol. Sci. 1998, 13:281-286.
25. Jessen C. Selective brain cooling in mammals and bird. Jpn. J. Physiol. 2001, 51:291-301.
26. Johnson J.I. Chapter 15. Comparative development of somatic sensory cortex. Cerebral Cortex Volume 8B. Comparative Structure and Evolution of Cerebral Cortex, Part II 1990, 335-449. Plenum Press, New York. E.G. Jones, A. Peters (Eds.).
27. 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. J. Chem. Neuroanat. 2010, 40:256-262.
28. Kuhnen G. Selective brain cooling reduces respiratory water loss during heat stress. Comp. Biochem. Physiol. A: Physiol. 1997, 118:891-895.
29. Lyamin O.I., Manger P.R., Ridgway S.H., Muhametov L.M., Siegel J.M. Cetacean sleep: an unusual form of mammalian sleep. Neurosci. Biobehav. Rev. 2008, 32:1451-1484.
30. Manger P.R. An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol. Rev. Camb. Philos. Soc. 2006, 81:293-338.
31. Manger P.R., Pillay P., Maseko B.C., Bhagwandin A., Gravett N., Moon D.J., Jillani N.E., Hemingway J. Acquisition of the brain of the African elephant (Loxodonta africana): perfusion-fixation and dissection. J. Neurosci. Methods 2009, 179:16-21.
32. Manger P.R., Prowse M., Haagensen M., Hemingway J. Quantitative analysis of neocortical gyrencephaly in African elephants (Loxodonta africana) and six species of cetaceans: comparison with other mammals. J. Comp. Neurol. 2012, 520:2430-2439.
33. Maseko B.C., Patzke N., Fuxe K., Manger P.R. Architectural organization of the African elephant diencephalon and brainstem. Brain Behav. Evol. 2013, 82:83-128.
34. McGregor R., Wu M.-F., Barber G., Ramanathan L., Siegel J.M. Highly specific role of hypocretin (orexin) neurons: differential activation as a function of diurnal phase, operant reinforcement vs. operant avoidance and light level. J. Neurosci. 2011, 31:15455-15467.
35. Mileykovskiy B.Y., Kiyashchenko L.I., Siegel J.M. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 2005, 46:787-798.
36. 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). J. Chem. Neuroanat. 2001, 21:225-238.
37. Mitchell D., Maloney S.K., Jessen C., Laburn H.P., Kamerman P.R., Mitchell G., Fuller A. Adaptive heterothermy and selective brain cooling in arid-zone mammals. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2002, 131:571-585.
38. Moore R.Y., Abrahamson E.A., van den Pol A. The hypocretin neuron system: an arousal system in the human brain. Arch. Ital. Biol. 2001, 139:195-206.
39. Nambu T., Sakurai T., Mizuhami K., Hosoya Y., Yanagisawa M., Goto K. Distribution of orexin neurons in the adult rat brain. Brain Res. 1999, 827:243-260.
40. 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. Behav. Brain Funct. 2007, 3:28.
41. Parsons M.P., Hirasawa M. ATP-sensitive potassium channel-mediated lactate effect on orexin neurons: implications for brain energetics during arousal. J. Neurosci. 2010, 30:8061-8070.
42. Patzke N., Bertelsen M.F., Fuxe K., Manger P.R. Nuclear organization of cholinergic, catecholaminergic, serotonergic and orexinergic systems in the brain of the Tasmanian devil (Sarcophilus harrisii). J. Chem. Neuroanat. 2014, 61-62:94-106.
43. Pellerin L., Magistretti P.J. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10625-10629.
44. 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. J. Neurosci. 1998, 18:9996-10015.
45. Pichon L., Huneau J., Fromentin G., Tomé D. A high-protein, high-fat, carbohydrate-free diet reduces energy intake, hepatic lipogenesis, and adiposity in rats. J. Nutr. 2006, 136:1256-1260.
46. Price S.A., Bininda-Emonds O.R., Gittleman J.L. A complete phylogeny of the whales, dolphins and even-toed hoofed mammals (Cetartiodactyla). Biol. Rev. Camb. Philos. Soc. 2005, 80:445-473.
47. Ridgway S.H., Brownson R.H. Relative brain sizes and cortical surface areas in odontocetes. ACTA Zool. Fenn. 1984, 172:149-152.
48. Ridgway S., Carder D., Finneran J., Keogh M., Kamolnick T., Todd M., Goldblatt A. Dolphin continuous auditory vigilance for five days. J. Exp. Biol. 2006, 209:3621-3628.
49. Ridgway S., Keogh M., Carder D., Finneran J., Kamolnick T., Todd M., Goldblatt A. Dolphins maintain cognitive performance during 72 to 120hours of continuous auditory vigilance. J. Exp. Biol. 2009, 212:1519-1527.
50. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., Williams S.C., Richardson J.A., Kozlowski G.P., Wilson S., Arch J.R.S., Buckingham R.E., Haynes A.C., Carr S.A., Annan R.S., McNulty D.E., Liu W.S., Terrett J.A., Elshourbagy N.A., Bergsma D.J., Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92:573-585.
51. Santos M.B., Pierce G.J. The diet of harbour porpoise (Phocoena phocoena) in the northeast Atlantic. Oceanogr. Mar. Biol. Ann. Rev. 2003, 41:355-390.
52. Schenker N.M., Hopkins W.D., Spocter M.A., Garrison A.R., Stimpson C.D., Erwin J.M., Hof P.R., Sherwood C.C. Broca's area homologue in chimpanzee (Pan troglodytes): probabilistic mapping, asymmetry, and comparison to humans. Cereb. Cortex 2010, 20:730-742.
53. Schmitz C., Hof P.R. Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J. Chem. Neuroanat. 2000, 20:93-114.
54. Song C., Chen X., Xia J., Yu Z., Hu Z. Modulatory effects of hypocretin-1/orexin-A with glutamate and γ-aminobutyric acid on freshly isolated pyramidal neurons from the rat prefrontal cortex. Neurosci. Lett. 2006, 399:101-105.
55. Spinazzi R., Andries P.G., Rossi G.P., Nussdorfer G.G. Orexins in the regulation of the hypothalamic-pituitary-adrenal axis. Pharmacol. Rev. 2006, 58:46-57.
56. Thannickal T.C., Lai Y.Y., Siegel J.M. Hypocretin (orexin) cell loss in Parkinson's disease. Brain 2007, 130:1586-1595.
57. Tobler I., Schwierin B. Behavioural sleep in the giraffe (Giraffa camelopardalis) in a zoological garden. J. Sleep Res. 1996, 5:21-32.
58. van den Pol A.N. Hypothalamic hypocretin (orexin): robust innervation of the spinal cord. J. Neurosci. 1999, 19:3171-3182.
59. 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 Res. Online 2000, 3:35-42.
60. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 1991, 231:482-497.
61. 2. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:10685-10690.
62. Yamada N., Katsuura G., Tatsuno I., Asaki T., Kawahara S., Ebihara K., Nakao K. Orexin decreases mRNA expressions of NMDA and AMPA receptor subunits in rat primary neuron circuits. Peptides 2008, 29:1582-1587.
63. Yamasaki H., LaBar K.S., McCarthy G. Dissociable prefrontal brain systems for attention and emotion. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11447-11451.
64. Yan J., He C., Xia J., Zhang D., Hu Z. Orexin-A excites pyramidal neurons in layer 2/3 of the rat prefrontal cortex. Neurosci. Lett. 2012, 520:92-97.
65. Yoshida K., McCormack S., España R.A., Crocker A., Scammell T.E. Afferents to the orexin neurons of the rat brain. J. Comp. Neurol. 2006, 494:845-861.