Advertisement

Journal of Ornithology

, Volume 153, Supplement 1, pp 235–243 | Cite as

Control of circadian activity of birds by the interaction of melatonin with 7α-hydroxypregnenolone, a newly discovered neurosteroid stimulating locomotion

  • Kazuyoshi TsutsuiEmail author
  • Shogo Haraguchi
  • Kazuhiko Inoue
  • Hitomi Miyabara
  • Saori Suzuki
  • Takayoshi Ubuka
Review

Abstract

Melatonin regulates diurnal locomotor rhythms in birds as well as in other vertebrates, but the molecular mechanism by which melatonin regulates locomotor activity is poorly understood. Here, we summarize new findings showing that 7α-hydroxypregnenolone, a previously undescribed avian neurosteroid, mediates melatonin action on diurnal locomotor rhythms in birds. Recently, 7α-hydroxypregnenolone was identified as a novel avian neurosteroid in Japanese quail Coturnix japonica brain. It was found that 7α-hydroxypregnenolone acutely stimulates quail locomotor activity. Subsequently, it was clarified that diurnal changes in 7α-hydroxypregnenolone synthesis occur in parallel with changes in locomotor activity in quail. Finally, it was demonstrated that melatonin depresses the synthesis of 7α-hydroxypregnenolone, thus providing a mechanism through which the nocturnal increase in melatonin regulates diurnal changes in locomotor activity. This review highlights a novel molecular mechanism controlling circadian activity of birds by the interaction of melatonin with 7α-hydroxypregnenolone, a newly discovered neurosteroid stimulating locomotion.

Keywords

Neurosteroids 7α-hydroxypregnenolone Cytochrome P450 Dopamine Locomotor activity Diurnal changes Quail 

Notes

Acknowledgments

This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science and Culture, Japan (18107002, 22132004 and 22227002 to K.T.).

References

  1. Akwa Y, Morfin RF, Robel P, Baulieu EE (1992) Neurosteroid metabolism: 7α-hydroxylation of dehydroepiandrosterone and pregnenolone by rat brain microsomes. Biochem J 288:959–964PubMedGoogle Scholar
  2. Ball GF, Casto JM, Balthazart J (1995) Autoradiographic localization of D1-like dopamine receptors in the forebrain of male and female Japanese quail and their relationship with immunoreactive tyrosine hydroxylase. J Chem Neuroanat 9:121–133PubMedCrossRefGoogle Scholar
  3. Balthazart J, Foidart A, Harada N (1990a) Immunocytochemical localization of aromatase in the brain. Brain Res 514:327–333PubMedCrossRefGoogle Scholar
  4. Balthazart J, Foidart A, Surlemont C, Vockel A, Harada N (1990b) Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: An immunocytochemical study. J Comp Neurol 301:276–288PubMedCrossRefGoogle Scholar
  5. Balthazart J, Foidart A, Surlemont C, Harada N (1991) Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors. J Neurobiol 22:143–157PubMedCrossRefGoogle Scholar
  6. Bardo MT, Bowling SL, Pierce RC (1990) Changes in locomotion and dopamine neurotransmission following amphetamine, haloperidol, and exposure to novel environmental stimuli. Psychopharmacology 101:338–343PubMedCrossRefGoogle Scholar
  7. Baulieu EE (1997) Neurosteroids: of the nervous system, by the nervous system, for the nervous system. Recent Prog Horm Res 52:1–32PubMedGoogle Scholar
  8. Beaujean D, Mensah-Nyagan AG, Do-Rego JL, Luu-The V, Pelletier G, Vaudry H (1999) Immunocytochemical localization and biological activity of hydroxysteroid sulfotransferase in the frog brain. J Neurochem 72:848–857PubMedCrossRefGoogle Scholar
  9. Bruzzone F, Do-Rego JL, Luu-The V, Pelletier G, Vallarino M, Vaudry H (2010) Immunohistochemical localization and biological activity of 3β-hydroxysteroid dehydrogenase and 5α-reductase in the brain of the frog, Rana esculenta, during development. J Chem Neuroanat 39:35–50PubMedCrossRefGoogle Scholar
  10. Bullock AE, Clark AL, Grady SR, Robinson SF, Slobe BS, Marks MJ, Collins AC (1997) Neurosteroids modulate nicotinic receptor function in mouse striatal and thalamic synaptosomes. J Neurochem 68:2412–2423PubMedCrossRefGoogle Scholar
  11. Cockrem JF, Follett BK (1985) Circadian rhythm of melatonin in the pineal gland of the Japanese quail (Coturnix coturnix japonica). J Endocrinol 107:317–324PubMedCrossRefGoogle Scholar
  12. Compagnone NA, Mellon SH (2000) Neurosteroids: biosynthesis and function of these novel neuromodulators. Front Neuroendocrinol 21:1–56PubMedCrossRefGoogle Scholar
  13. Compagnone NA, Bulfone A, Rubenstein JL, Mellon SH (1995) Steroidogenic enzyme P450c17 is expressed in the embryonic central nervous system. Endocrinology 136:5212–5223PubMedCrossRefGoogle Scholar
  14. Corpéchot C, Robel P, Axelson M, Sjövall J, Baulieu EE (1981) Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc Natl Acad Sci USA 78:4704–4707PubMedCrossRefGoogle Scholar
  15. Corpéchot C, Synguelakis M, Talha S, Axelson M, Sjövall J, Vihko R, Baulieu EE, Robel P (1983) Pregnenolone and its sulfate ester in rat brain. Brain Res 270:119–125PubMedCrossRefGoogle Scholar
  16. Doostzadeh J, Morfin R (1997) Effects of cytochrome P450 inhibitors and of steroid hormones on the formation of 7-hydroxylated metabolites of pregnenolone in mouse brain microsomes. J Endocrinol 155:343–350PubMedCrossRefGoogle Scholar
  17. Do-Rego JL, Tremblay Y, Luu-The V, Repello E, Vallarino M, Belanger A, Pelletier G, Vaudry H (2007) Immunocytochemical localization and biological activity of the steroidogenic enzyme cytochrome P450 17α-hydroxylase/C17, 20-lyase (P450C17) in the frog brain and pituitary. J Neurochem 100:251–268PubMedCrossRefGoogle Scholar
  18. Do-Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, Tsutsui K, Tonon MC, Pelletier G, Vaudry H (2009) Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol 30:259–301PubMedCrossRefGoogle Scholar
  19. Freking F, Nazairians T, Schlinger BA (2000) The expression of the sex steroid-synthesizing enzymes CYP11A1, 3β-HSD, CYP17, and CYP 19 in gonads and adrenals of adult and developing zebra finches. Gen Comp Endocrinol 119:140–151PubMedCrossRefGoogle Scholar
  20. Fusani L, Cardinale M, Schwabl I, Goymann W (2011) Food availability but not melatonin affects nocturnal restlessness in a wild migrating passerine. Horm Behav 59:187–192PubMedCrossRefGoogle Scholar
  21. Gaston S, Menaker M (1968) Pineal function: the biological clock in the sparrow? Science 160:1125–1127PubMedCrossRefGoogle Scholar
  22. Gwinner E, Benzinger I (1978) Synchronization of a circadian rhythm in pinealectomized European starlings by daily injections of melatonin. J Comp Physiol 126:123–129CrossRefGoogle Scholar
  23. Gwinner E, Hau M, Heigl S (1997) Melatonin: generation and modulation of avian circadian rhythms. Brain Res Bull 44:439–444PubMedCrossRefGoogle Scholar
  24. Hara E, Kubikova L, Hessler NA, Jarvis ED (2007) Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur J Neurosci 25:3406–3416PubMedCrossRefGoogle Scholar
  25. Haraguchi S, Koyama T, Hasunuma I, Vaudry H, Tsutsui K (2010) Prolactin increases the synthesis of 7α-hydroxypregnenolone, a key factor for induction of locomotor activity, in breeding male newts. Endocrinology 151:2211–2222PubMedCrossRefGoogle Scholar
  26. Inai Y, Nagai K, Ukena K, Oishi T, Tsutsui K (2003) Seasonal changes in neurosteroids in the urodele brain and environmental factors inducing their changes. Brain Res 959:214–225PubMedCrossRefGoogle Scholar
  27. Iwata T, Toyoda F, Yamamoto K, Kikuyama S (2000) Hormonal control of urodele reproductive behavior. Comp Biochem Physiol B Biochem Mol Biol 126:221–229PubMedCrossRefGoogle Scholar
  28. Jo DH, Abdallah MA, Young J, Baulieu EE, Robel P (1989) Pregnenolone, dehydroepiandrosterone, and their sulfate and fatty acid esters in the rat brain. Steroids 54:287–297PubMedCrossRefGoogle Scholar
  29. Kumar V, Follett BK (1993) The circadian nature of melatonin secretion in Japanese quail (Coturnix coturnix japonica). J Pineal Res 14:192–200PubMedCrossRefGoogle Scholar
  30. Lambert JJ, Belelli D, Hill-Venning C, Peters JA (1995) Neurosteroids and GABAA receptor function. Trends Pharmacol Sci 16:295–303PubMedCrossRefGoogle Scholar
  31. Laviolette SR, van der Kooy D (2001) GABAA receptors in the ventral tegmental area control bidirectional reward signalling between dopaminergic and non-dopaminergic neural motivational systems. Eur J Neurosci 13:1009–1015PubMedCrossRefGoogle Scholar
  32. Lea RW, Clark JA, Tsutsui K (2001) Changes in central steroid receptor expression, steroid synthesis and dopaminergic activity related to the reproductive cycle of the ring dove (review). Microsc Res Tech 55:12–26PubMedCrossRefGoogle Scholar
  33. Levens N, Green TA, Akins CK, Bardo MT (2000) Dopamine D2-like receptor binding in the brain of male Japanese quail (Coturnix japonica). Neurosci Lett 22:77–80CrossRefGoogle Scholar
  34. London SE, Schlinger BA (2007) Steroidogenic enzymes along the ventricular proliferative zone in the developing songbird brain. J Comp Neurol 502:507–521PubMedCrossRefGoogle Scholar
  35. London SE, Boulter J, Schlinger BA (2003) Cloning of the zebra finch androgen synthetic enzyme CYP17: a study of its neural expression throughout posthatch development. J Comp Neurol 467:496–508PubMedCrossRefGoogle Scholar
  36. London SE, Monks DA, Wade J, Schlinger BA (2006) Widespread capacity for steroid synthesis in the avian brain and song system. Endocrinology 147:5975–5987PubMedCrossRefGoogle Scholar
  37. London SE, Remage-Healey L, Schlinger BA (2009) Neurosteroid production in the songbird brain: a re-evaluation of core principles. Front Neuroendocrinol 30:302–314PubMedCrossRefGoogle Scholar
  38. London SE, Itoh Y, Lance VA, Wise PM, Ekanayake PS, Oyama RK, Arnold AP, Schlinger BA (2010) Neural expression and post-transcriptional dosage compensation of the steroid metabolic enzyme 17β-HSD type 4. BMC Neurosci 11:47PubMedCrossRefGoogle Scholar
  39. Massa R, Sharp PJ (1981) Conversion of testosterone to 5β-reduced metabolites in the neuroendocrine tissues of the maturing cockerel. J Endocrinol 88:263–269PubMedCrossRefGoogle Scholar
  40. Mathur C, Prasad VV, Raju VS, Welch M, Lieberman S (1993) Steroids and their conjugates in the mammalian brain. Proc Natl Acad Sci USA 90:85–88PubMedCrossRefGoogle Scholar
  41. Matsunaga M, Ukena K, Tsutsui K (2001) Expression and localization of the cytochrome P450 17α-hydroxylase/c17, 20-lyase in the avian brain. Brain Res 899:112–122PubMedCrossRefGoogle Scholar
  42. Matsunaga M, Ukena K, Tsutsui K (2002) Androgen biosynthesis in the quail brain. Brain Res 948:180–185PubMedCrossRefGoogle Scholar
  43. Matsunaga M, Ukena K, Baulieu EE, Tsutsui K (2004) 7α-Hydroxypregnenolone acts as a neuronal activator to stimulate locomotor activity of breeding newts by means of the dopaminergic system. Proc Natl Acad Sci USA 101:17282–17287PubMedCrossRefGoogle Scholar
  44. Mellon SH, Deschepper CF (1993) Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res 629:283–292PubMedCrossRefGoogle Scholar
  45. Mellon SH, Vaudry H (2001) Biosynthesis of neurosteroids and regulation of their synthesis. Int Rev Neurobiol 46:33–78PubMedCrossRefGoogle Scholar
  46. Mensah-Nyagan AG, Feuilloley M, Dupont E, Do-Rego JL, Leboulenger F, Pelletier G, Vaudry H (1994) Immunocytochemical localization and biological activity of 3β-hydroxysteroid dehydrogenase in the central nervous system of the frog. J Neurosci 14:7306–7318PubMedGoogle Scholar
  47. Mensah-Nyagan AG, Feuilloley M, Do-Rego JL, Marcual A, Lange C, Tonon MC, Pelletier G, Vaudry H (1996) Localization of 17β-hydroxysteroid dehydrogenase and characterization of testosterone in the brain of the male frog. Proc Natl Acad Sci USA 93:1423–1428PubMedCrossRefGoogle Scholar
  48. Mensah-Nyagan AG, Do-Rego JL, Beaujean D, Luu-The V, Pelletier G, Vaudry H (1999) Neurosteroids: expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system (review). Pharmacol Rev 51:63–81PubMedGoogle Scholar
  49. Mezey S, Csillag A (2002) Selective striatal connections of midbrain dopaminergic nuclei in the chick (Gallus domesticus). Cell Tissue Res 308:35–46PubMedCrossRefGoogle Scholar
  50. Murakami N, Kawano T, Nakahara K, Nasu T, Shiota K (2001) Effect of melatonin on circadian rhythm, locomotor activity and body temperature in the intact house sparrow, Japanese quail and owl. Brain Res 889:220–224PubMedCrossRefGoogle Scholar
  51. Nakahara K, Kawano T, Shiota K, Murakami N (2003) Effects of microinjection of melatonin into various brain regions of Japanese quail on locomotor activity and body temperature. Neurosci Lett 345:117–120PubMedCrossRefGoogle Scholar
  52. Paul SM, Purdy RH (1992) Neuroactive steroids. FASEB J 6:2311–2322PubMedGoogle Scholar
  53. Peterson RS, Yarram L, Schlinger BA, Saldanha CJ (2005) Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain. Proc R Soc Lond B 272:2089–2096CrossRefGoogle Scholar
  54. Remage-Healey L, Maidment NT, Schlinger BA (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327–1334PubMedCrossRefGoogle Scholar
  55. Remage-Healey L, Oyama RK, Schlinger BA (2009) Elevated aromatase activity in forebrain synaptic terminals during song. J Neuroendocrinol 21:191–199PubMedCrossRefGoogle Scholar
  56. Remage-Healey L, London SE, Schlinger BA (2010) Birdsong and the neural production of steroids. J Chem Neuroanat 39:72–81PubMedCrossRefGoogle Scholar
  57. Robel P, Baulieu EE (1985) Neuro-steroids, 3β-hydroxy-∆5-derivatives in the rodent brain. Neurochem Int 7:953–958PubMedCrossRefGoogle Scholar
  58. Robel P, Bourreau E, Corpéchot C, Dang DC, Halberg F, Clarke C, Haug M, Schlegel ML, Synguelakis M, Vourch C et al (1987) Neuro-steroids: 3β-hydroxy-∆5-derivatives in rat and monkey brain. J Steroid Biochem 27:649–655PubMedCrossRefGoogle Scholar
  59. Rougé-Pont F, Mayo W, Marinelli M, Gingras M, Moal ML, Piazza PV (2002) The neurosteroid allopregnanolone increases dopamine release and dopaminergic response to morphine in the rat nucleus accumbens. Eur J Neurosci 16:169–173PubMedCrossRefGoogle Scholar
  60. Sakamoto H, Ukena K, Tsutsui K (2001) Activity and localization of 3β-hydroxysteroid dehydrogenase/∆5-∆4-isomerase in the zebrafish central nervous system. J Comp Neurol 439:291–305PubMedCrossRefGoogle Scholar
  61. Sanberg PR (1983) Dopaminergic and cholinergic influences on motor behavior in chickens. J Comp Psychol 97:59–68PubMedCrossRefGoogle Scholar
  62. Schlinger BA, Callard GV (1987) A comparison of aromatase, 5α, and 5β-reductase activities in the brain and pituitary of male and female quail (Coturnix coturnix japonica). J Exp Zool 242:171–180PubMedCrossRefGoogle Scholar
  63. Schlinger BA, Callard GV (1989) Aromatase activity in quail brain: Correlation with aggressiveness. Endocrinology 124:437–443PubMedCrossRefGoogle Scholar
  64. Schlinger BA, Lane NI, Grisham W, Thompson L (1999) Androgen synthesis in a songbird: a study of cyp17 (17α-hydroxylase/c17, 20-lyase) activity in the zebra finch. Gen Comp Endocrinol 113:46–58PubMedCrossRefGoogle Scholar
  65. Sharp T, Zetterström T, Ljungberg T, Ungerstedt U (1987) A direct comparison of amphetamine-induced behaviours and regional brain dopamine release in the rat using intracerebral dialysis. Brain Res 401:322–330PubMedCrossRefGoogle Scholar
  66. Soma KK, Alday NA, Hau M, Schlinger BA (2004) Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/Δ54-isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 145:1668–1677PubMedCrossRefGoogle Scholar
  67. Takase M, Ukena K, Yamazaki T, Kominami S, Tsutsui K (1999) Pregnenolone, pregnenolone sulfate and cytochrome P450 side-chain cleavage enzyme in the amphibian brain and their seasonal changes. Endocrinology 140:1936–1944PubMedCrossRefGoogle Scholar
  68. Takase M, Ukena K, Tsutsui K (2002) Expression and localization of cytochrome P45011β, aldo mRNA in the frog brain. Brain Res 950:288–296PubMedCrossRefGoogle Scholar
  69. Takase M, Haraguchi S, Hasunuma I, Kikuyama S, Tsutsui K (2011) Expression of cytochrome P450 side-chain cleavage enzyme mRNA in the brain of the Red-bellied newt Cynops pyrrhogaster. Gen Comp Endocrinol 170:468–474PubMedCrossRefGoogle Scholar
  70. Tam H, Schlinger BA (2007) Activities of 3β-HSD and aromatase in slices of developing and adult zebra finch brain. Gen Comp Endocrinol 150:26–33PubMedCrossRefGoogle Scholar
  71. Tsutsui Y (1931) Notes on the behavior of the common Japanese newt, Diemyctylus pyrrhogaster BOIE. I. Breeding habit. Mem Col Sci Kyoto Imp Univ Ser B7:159–179Google Scholar
  72. Tsutsui K, Schlinger BA (2001) Steroidogenesis in the avian brain. In: Dawson A, Chaturvedi CM (eds) Avian endocrinology. Narosa, New Delhi, pp 59–77Google Scholar
  73. Tsutsui K, Yamazaki T (1995) Avian neurosteroids. I. Pregnenolone biosynthesis in the quail brain. Brain Res 678:1–9PubMedCrossRefGoogle Scholar
  74. Tsutsui K, Ukena K, Takase M, Kohchi C, Lea RW (1999) Review: neurosteroid biosynthesis in vertebrate brains. Comp Biochem Physiol C 124:121–129PubMedGoogle Scholar
  75. Tsutsui K, Matsunaga M, Ukena K (2003) Review: Biosynthesis and biological actions of neurosteroids in the avian brain. Avian Poult Biol Rev 14:63–78CrossRefGoogle Scholar
  76. Tsutsui K, Matsunaga M, Miyabara H, Ukena K (2006) Review: Neurosteroid biosynthesis in the quail brain. J Exp Zool 305:733–742CrossRefGoogle Scholar
  77. Tsutsui K, Inoue K, Miyabara H, Suzuki S, Ogura Y, Haraguchi S (2008) 7α-Hydroxypregnenolone mediates melatonin action underlying diurnal locomotor rhythms. J Neurosci 28:2158–2167PubMedCrossRefGoogle Scholar
  78. Tsutsui K, Haraguchi S, Matsunaga M, Inoue K, Vaudry H (2010) Review: 7α-Hydroxypregnenolone, a new key regulator of locomotor activity of vertebrates: Identification, mode of action and functional significance. Front Endocrinol 1(9):1–13Google Scholar
  79. Ukena K, Honda Y, Inai Y, Kohchi C, Lea RW, Tsutsui K (1999) Expression and activity of 3β-hydroxysteroid dehydrogenase/Δ54-isomerase in different regions of the avian brain. Brain Res 818:536–542PubMedCrossRefGoogle Scholar
  80. Ukena K, Honda Y, Lea RW, Tsutsui K (2001) Developmental changes in progesterone biosynthesis and metabolism in the quail brain. Brain Res 898:190–194PubMedCrossRefGoogle Scholar
  81. Underwood H (1994) The circadian rhythm of thermoregulation in Japanese quail. I. Role of the eyes and pineal. J Comp Physiol A 175:639–653Google Scholar
  82. Underwood H, Binkley S, Siopes T, Mosher K (1984) Melatonin rhythms in the eyes, pineal bodies, and blood of Japanese quail (Coturnix coturnix japonica). Gen Comp Endocrinol 56:70–81PubMedCrossRefGoogle Scholar
  83. Underwood H, Steele CT, Zivkovic B (2001) Circadian organization and the role of the pineal in birds. Microsc Res Tech 53:48–62PubMedCrossRefGoogle Scholar
  84. Usui M, Yamazaki T, Kominami S, Tsutsui K (1995) Avian neurosteroids. II. Localization of a cytochrome P450scc-like substance in the quail brain. Brain Res 678:10–20PubMedCrossRefGoogle Scholar
  85. Vanson A, Arnold AP, Schlinger BA (1996) 3β-Hydroxysteroid dehydrogenase/isomerase and aromatase activity in primary cultures of developing zebra finch telencephalon: dehydroepiandrosterone as substrate for synthesis of androstenedione and estrogens. Gen Comp Endocrinol 102:342–350PubMedCrossRefGoogle Scholar
  86. Wada M (1979) Photoperiodic control of LH secretion in Japanese quail with special reference to the photoinducible phase. Gen Comp Endocrinol 39:141–149PubMedCrossRefGoogle Scholar
  87. Weill-Engerer S, David J-P, Sazdovitche V, Lierea P, Schumachera M, Delacourte A, Baulieu E-E, Akwa Y (2003) In vitro metabolism of dehydroepiandrosterone (DHEA) to 7α-hydroxy-DHEA and Δ5-androstene-3β,17β-diol in specific regions of the aging brain from Alzheimer’s and non-demented patients. Brain Res 969:117–125Google Scholar
  88. Wieland S, Belluzzi JD, Stein L, Lan NC (1995) Comparative behavioral characterization of the neuroactive steroids 3 alpha–OH, 5 alpha-pregnan-20-one and 3 alpha–OH, 5 beta-pregnan-20-one in rodents. Psychopharmacology 118:65–71PubMedCrossRefGoogle Scholar
  89. Wilson WO (1972) A review of the physiology of Coturnix (Japanese quail). World Poult Sci J 28:413–429CrossRefGoogle Scholar
  90. Yau JL, Rasmuson S, Andrew R, Graham M, Noble J, Olsson T, Fuchs E, Lathe R, Seckl JR (2003) Dehydroepiandrosterone 7-hydroxylase CYP7B: predominant expression in primate hippocampus and reduced expression in Alzheimer’s disease. Neuroscience 121:307–314PubMedCrossRefGoogle Scholar
  91. Zimmerman NH, Menaker M (1979) The pineal gland: a pacemaker within the circadian system of the house sparrow. Proc Natl Acad Sci USA 76:999–1003PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2011

Authors and Affiliations

  • Kazuyoshi Tsutsui
    • 1
    Email author
  • Shogo Haraguchi
    • 1
  • Kazuhiko Inoue
    • 1
  • Hitomi Miyabara
    • 2
  • Saori Suzuki
    • 2
  • Takayoshi Ubuka
    • 1
  1. 1.Laboratory of Integrative Brain Sciences, Department of BiologyWaseda University, Center for Medical Life Science of Waseda UniversityTokyoJapan
  2. 2.Laboratory of Brain Science, Faculty of Integrated Arts and SciencesHiroshima UniversityHigashi-HiroshimaJapan

Personalised recommendations