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Impact of Micro- and Hypergravity on Neurovestibular Issues of Fish

  • R. W. HilbigEmail author
  • R. H. Anken
Chapter
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Part of the SpringerBriefs in Space Life Sciences book series (BRIEFSSLS)

Abstract

For decades, research in altered gravitational environments has been undertaken to elucidate the impact of gravity on a broad variety of biosystems from unicellular organisms to vertebrate animals. In the preparation of scarce and costly orbital missions, different short-term flight opportunities (drop-tower flights, parabolic aircraft flights, sounding rocket flights) as well as ground-based facilities like centrifuges and microgravity simulators are being used. Here, we present an overview of studies carried out under short-term and long-term altered gravity on fish, with a focus on vestibular issues of cichlid fish (Oreochromis mossambicus) larvae and juvenile swordtails (Xiphophorus helleri). These experiments were focused on their behaviour, analyses of neuronal tissues, epithelia of utricle and saccule and as well on inner ear stones, the otoliths. Kinetoses (motion sickness) were frequently observed in altered—especially diminished—gravity, and evidence could be provided that asymmetric otoliths are a major factor in kinetosis susceptibility. Furthermore, we could show that the biomineralization of otoliths is adjusted towards gravity by means of a neuronally guided feedback loop.

Keywords

Fish Inner ear Otolith Calcium Bio mineralization Asymmetry Behaviour Kinetosis Space Microgravity Drop tower Texus 
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Notes

Acknowledgements

The authors would like to thank the German Space Administration (DLR) for funding and co-ordinating our space-related research projects (Grant 50WB0527, 50WB1027) and the teams of ESA, ZARM, Novespace and SSC (Swedish Space Corporation) for their valuable support in the preparation phase and during the missions.

References

  1. Aceto J, Nourizadeh-Lillabadi R, Marée R et al (2015) Zebrafish bone and general physiology are differently affected by hormones or changes in gravity. PLoS One 10(6):e0126928. https://doi.org/10.1371/journal.pone.0126928 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anken RH (2006) On the role of the central nervous system in regulating the mineralization of inner-ear otoliths of fish. Protoplasma 229:205–208. https://doi.org/10.1007/s00709-006-0219-6 CrossRefPubMedGoogle Scholar
  3. Anken RH, Hilbig R (2004) Determination of the threshold of gravity for inducing kinetosis in fish: a drop-tower experiment. Microgravity Sci Technol 15:52–57. https://doi.org/10.1007/BF02870958 CrossRefPubMedGoogle Scholar
  4. Anken RH, Rahmann H (1999) Effect of altered gravity on the neurobiology of fish. Naturwissenschaften 86:155–167CrossRefPubMedGoogle Scholar
  5. Anken RH, Rahmann H (2002) Gravitational zoology: how animals use and cope with gravity. In: Horneck G, Baumstark-Khan C (eds) Astrobiology. Springer, Berlin, pp 315–333CrossRefGoogle Scholar
  6. Anken RH, Kappel T, Slenzka K et al (1993) The early morphogenetic development of the chichlid fish, Oreochromis mossambicus (Perciformes, Teleostei). Zool Anz 231:1–10Google Scholar
  7. Anken RH, Ibsch M, Rahmann H (1998a) Neurobiology of fish under altered gravity conditions. Brain Res Rev 28:9–18CrossRefPubMedGoogle Scholar
  8. Anken RH, Kappel T, Rahmann H (1998b) Morphometry of fish inner ear otoliths after development at 3g hypergravity. Acta Otolaryngol 118:534–539CrossRefPubMedGoogle Scholar
  9. Anken RH, Hilbig R, Ibsch M et al (1999) Readaptation of fish to 1g after long-term microgravity—neurobiological results from the STS 89 and the STS 90- (Neurolab) mission. In: Proceedings of the 7th European symposium on life sciences research in space, pp 124–126Google Scholar
  10. Anken RH, Edelmann E, Rahmann H (2000) Fish inner ear otoliths stop calcium incorporation after vestibular nerve transection. Neuroreport 11:2981–2983CrossRefPubMedGoogle Scholar
  11. Anken RH, Ibsch M, Breuer J et al (2001) Effect of hypergravity on the Ca/Sr composition of developing otoliths of larval cichlid fish (Oreochromis mossambicus). Comp Biochem Physiol A 128:369–377CrossRefGoogle Scholar
  12. Anken RH, Beier M, Edelmann E et al (2002) Neuronal regulation of otolith growth and kinetotic behaviour. J Gravit Physiol 9:37–38Google Scholar
  13. Anken RH, Beier M, Rahmann H (2004) Hypergravity decreases carbonic anhydrase-reactivity in inner ear maculae of fish. J Exp Zool A 301:815–819CrossRefGoogle Scholar
  14. Anken RH, Forster A, Baur U et al (2006) Otolith asymmetry and kinetotic behaviour of fish at high-quality microgravity: a drop-tower experiment. Adv Space Res 38:1032–1036CrossRefGoogle Scholar
  15. Anken RH, Baur U, Hilbig R (2010) Clinorotation increases the growth of utricular otoliths of developing cichlid fish. Microgravity Sci Technol 22:151–154CrossRefGoogle Scholar
  16. Anken RH, Brungs S, Grimm D et al (2016) Fish inner ear otolith growth under real microgravity (spaceflight) and clinorotation. Microgravity Sci Technol 28:351–356CrossRefGoogle Scholar
  17. Baird L (1974) Anatomical features of the inner ear in submammalian vertebrates. In: Keidel W, Neff W (eds) Auditory system: anatomy physiology (ear). Springer, New York, pp 159–212CrossRefGoogle Scholar
  18. Bäuerle A, Anken RH, Hilbig R et al (2004a) Histology of the utricle in kinetotically swimming fish: a parabolic aircraft flight study. Acta Otolaryngol 124:19–22CrossRefPubMedGoogle Scholar
  19. Bäuerle A, Anken RH, Hilbig R et al (2004b) Size and cell number of the utricle in kinetotically swimming fish: a parabolic aircraft flight study. Adv Space Res 34:1598–1601CrossRefPubMedGoogle Scholar
  20. Beier M, Anken RH (2006) On the role of carbonic anhydrase in the early phase of fish otolith mineralization. Adv Space Res 38:1119–1122CrossRefGoogle Scholar
  21. Beier M, Anken RH, Rahmann H (2002a) Influence of hypergravity on fish inner ear otoliths: II. Incorporation of calcium and kinetotic behaviour. Adv Space Res 30:727–731CrossRefPubMedGoogle Scholar
  22. Beier M, Anken RH, Rahmann H (2002b) Susceptibility to abnormal (kinetotic). Swimming fish correlates with inner ear carbonic anhydrase-reactivity. Neurosci Lett 335:17–20CrossRefPubMedGoogle Scholar
  23. Beier M, Hilbig R, Anken RH (2008) Histochemical localisation of carbonic anhydrase in the inner ear of developing cichlid fish, Oreochromis mossambicus. Adv Space Res 42:1986–1994CrossRefGoogle Scholar
  24. Blüm V (2003) Aquatic modules for bioregenerative life support systems: developmental aspects based on the space flight results of the C.E.B.A.S. MINI-MODULE. Adv Space Res 31:1683–1691CrossRefPubMedGoogle Scholar
  25. Blüm V, Paris F (2001) Aquatic modules for bioregenerative life support systems based on the C.E.B.A.S. Biotechnology. Acta Astronaut 48:287–297CrossRefGoogle Scholar
  26. Blüm V, Andriske M, Ludwig C et al (2003) The “C.E.B.A.S. MINI-MODULE”: a self-sustaining closed aquatic ecosystem for spaceflight experimentation. Adv Space Res 2003:201–210CrossRefGoogle Scholar
  27. Briegleb W, Neubert J, Schatz A et al (1986) Survey of the vestibulum, and behavior of Xenopus laevis larvae developed during a 7-days space flight. Adv Space Res 6:151–156CrossRefPubMedGoogle Scholar
  28. Brungs S, Hauslage J, Hilbig R et al (2011) Effects of simulated weightlessness on fish otolith growth: clinostat versus rotating-wall vessel. Adv Space Res 48:792–798CrossRefGoogle Scholar
  29. Casper B (2011) The ear and hearing in sharks, skates, and rays. In: Farrell A (ed) Encyclopedia of fish physiology: from genome to environment. Academic Press, San Diego, pp 262–269CrossRefGoogle Scholar
  30. Davis J, Oberholtzer J, Burns F et al (1995) Molecular cloning and characterization of an inner ear-specific protein. Science 267:1031–1034CrossRefPubMedGoogle Scholar
  31. Davis J, Burns F, Navaratnam D et al (1997) Identification of a structural constituent and one possible site of postembryonic formation of a teleost otolithic membrane. Proc Natl Acad Sci U S A 94:707–712CrossRefPubMedPubMedCentralGoogle Scholar
  32. DeJong H, Sondag E, Kuipers A et al (1996) Swimming behaviour of fish during short periods of weightlessness. Aviat Space Environ Med 67:463–466Google Scholar
  33. Dumont RA, Lins U, Filoteo AG et al (2001) Plasma membrane Ca2+-ATPase isoform 2a is the PMCA of hair bundles. J Neurosci 21(14):5066–5078PubMedGoogle Scholar
  34. Edelmann E, Anken RH, Rahmann H (2004) Swimming behaviour and calcium incorporation into inner ear otoliths of fish after vestibular nerve transection. Adv Space Res 33:1390–1394CrossRefPubMedGoogle Scholar
  35. Fermin CD, Lychakov D, Campos A et al (1998) Otoconia biogenesis, phylogeny, composition and functional attributes. Histol Histopathol 13:1103–1154PubMedGoogle Scholar
  36. Fritzsch B (1992) The water-to-land transition: evolution of the tetrapod basilar papilla, middle ear and auditory nuclei. In: Webster D, Fay R, Popper A (eds) The evolutionary biology of hearing. Springer, New York, pp 351–375CrossRefGoogle Scholar
  37. Fritzsch B (1998) Evolution of the vestibulo-ocular system. Otolaryngol Head Neck Surg 119:182–192CrossRefPubMedGoogle Scholar
  38. Fritzsch B, Beisel K, Jones K et al (2002) Development and evolution of inner ear sensory epithelia and their innervation. J Neurobiol 53:143–156. https://doi.org/10.1002/neu.10098 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Häder D, Braun M, Grimm D et al (2017) Gravireceptors in eukaryotes—a comparison of case studies on the cellular level. NPJ Microgravity 3:13. https://doi.org/10.1038/s41526-017-0018-8 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Helling K, Hausmann S, Clark A et al (2003) Experimentally induced motion sickness in fish: possible role of the otolith organs. Acta Otolaryngol 123:488–492CrossRefPubMedGoogle Scholar
  41. Herranz R, Anken RH, Boonstra J et al (2013) Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology 13:1–17CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hilbig R, Lebert M (2010) OMEGAHAB-XP a bioregenerative aquatic life support system designed to be used in Bion-M1 long term space flight. In: Abstracts of the proceedings of the 38th COSPAR scientific assembly, Code: 2010cosp...38.3359HGoogle Scholar
  43. Hilbig R, Schüle T, Ibsch M et al (1996) New approaches to the gravity relevant behavior of the swordtail fish (Xiphophorus helleri). In: Proceedings of the XII. C.E.B.A.S. Workshop conference, pp 51–57Google Scholar
  44. Hilbig R, Anken RH, Bäuerle A et al (2002a) Susceptibility to motion sickness in fish: a parabolic aircraft flight study. J Gravit Physiol 8:29–30Google Scholar
  45. Hilbig R, Anken RH, Sonntag G et al (2002b) Effects of altered gravity on the swimming behavior of fish. Adv Space Res 30:835–841CrossRefPubMedGoogle Scholar
  46. Hilbig R, Anken RH, Rahmann H (2003) On the origin of susceptibility to kinetotic swimming behaviour in fish: a parabolic aircraft flight study. J Vestib Res 12:185–189Google Scholar
  47. Hilbig R, Knie M, Shcherbakov D et al. (2011) Analysis of behaviour and habituation of fish exposed to diminished gravity in correlation to inner ear stone formation: a sounding rocket experiment (Texus 45). In: Proceedings of the 20th ESA symposium on European rocket and balloon programmes and related research, ESA SP-700, p 6Google Scholar
  48. Hoffman R, Salinas G, Baky A (1977) Behavioral analyses of killifish exposed to weightlessness in the Apollo-Soyuz test project. Aviat Space Environ Med 48:712–717PubMedGoogle Scholar
  49. Horn E, Sebastian C (2002) Adaptation of the macular vestibule ocular reflex to altered gravitational conditions in a fish (Oreochromis mossambicus). Adv Space Res 30:711–720CrossRefPubMedGoogle Scholar
  50. Hudspeth A (2008) Making an effort to listen: mechanical amplification in the ear. Neuron 59:530–545. https://doi.org/10.1016/j.neuron.2008.07.012 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hughes I, Thalmann I, Thalmann R et al (2006) Mixing model systems: using zebrafish and mouse inner ear mutants and other organ systems to unravel the mystery of otoconial development. Brain Res 1091:58–74CrossRefPubMedPubMedCentralGoogle Scholar
  52. Ibsch M, Anken RH, Rahmann H (2004) Calcium gradients in the fish inner ear sensory epithelium and otolithic membrane visualized by energy filtering transmission electron microscopy (EFTEM). Adv Space Res 33:1395–1400CrossRefPubMedGoogle Scholar
  53. Ijiri K (1995) Fish mating experiment in space—what it aimed at and how it was prepared. Biol Sci Space 9:3–16CrossRefPubMedGoogle Scholar
  54. Knie M (2014) Zur Lokalisation und Funktion des Calciumtransporters im Innenohr von Knochenfischen (Oreochromis mossambicus). PhD-thesis, Institute of Zoology, University of Hohenheim, StuttgartGoogle Scholar
  55. Kohn F, Hauslage J, Hanke W (2017) Membrane fluidity changes, a basic mechanism of interaction of gravity with cells? Microgravity Sci Technol. https://doi.org/10.1007/s12217-017-9552-y
  56. Ladich F, Schulz-Mirbach T (2016) Diversity in fish auditory systems: one of the riddles of sensory biology. Front Ecol Evol 4:article 28. https://doi.org/10.3389/fevo.2016.00028 CrossRefGoogle Scholar
  57. Li X, Anken RH, Wang G et al (2011) Effects of wall vessel rotation on the growth of larval zebrafish inner ear otoliths. Microgravity Sci Technol 23:13–18CrossRefGoogle Scholar
  58. Li X, Anken RH, Liu L et al (2017) Effects of simulated microgravity on otolith growth of larval zebrafish using a rotating-wall vessel: appropriate rotation speed and fish developmental stage. Microgravity Sci Technol 29:1–8CrossRefGoogle Scholar
  59. Lowenstein O, Roberts T (1949) The equilibrium function of the otolith organs of the thornback ray (Raja clavata). J Physiol 110:392–415CrossRefPubMedPubMedCentralGoogle Scholar
  60. Miller-Bever M, Fekete DM (2002) Atlas of the developing inner ear in zebrafish. Dev Dyn 223:536–543. https://doi.org/10.1002/dvdy.10062 CrossRefGoogle Scholar
  61. Mori S, Mitarai G, Takabayashi A et al (1996) Evidence of sensory conflict and recovery in carp exposed to prolonged weightlessness. Aviat Space Environ Med 67:256–261PubMedGoogle Scholar
  62. Murayama E, Takagi Y, Nagasawa H (2004) Immunohistochemical localization of two otolith matrix proteins in the otolith and inner ear of the rainbow trout, Oncorhynchus mykiss: comparative aspects between the adult inner ear and embryonic otocysts. Histochem Cell Biol 121:155–166CrossRefPubMedGoogle Scholar
  63. Murayama E, Herbomel P, Kawakami A et al (2005) Otolith matrix proteins OMP-1 and Otolin-1 are necessary for normal otolith growth and their correct anchoring onto the sensory maculae. Mech Dev 122:791–803CrossRefPubMedGoogle Scholar
  64. Parker D (1998) The relative roles of the otolith organs and semicircular canals in producing space motion sickness. J Vest Res 8:57–59CrossRefGoogle Scholar
  65. Petko J, Millimaki B, Canfield V et al (2008) Otoc1: a novel otoconin-90 ortholog required for otolith mineralization in zebrafish. Dev Neurobiol 68:209–222CrossRefPubMedPubMedCentralGoogle Scholar
  66. Platt C (1983) The peripheral vestibular system of fishes. In: Northcutt R, Davis R (eds) Fish neurobiology. University of Michigan Press, Ann Arbor, pp 89–123Google Scholar
  67. Popper A (1981) Comparative scanning electron microscopic investigations of the sensory epithelia in the teleost sacculus and lagena. J Comp Neurol 200:357–374CrossRefPubMedGoogle Scholar
  68. Popper A, Fay R (1993) Sound detection and processing by fish-critical review and major research questions. Brain Behav Evol 41:14–38. https://doi.org/10.1159/000113821 CrossRefPubMedGoogle Scholar
  69. Porst M, Lebert M, Häder D (1997) Long-term cultivation of the flagellate Euglena gracilis. Microgravity Sci Technol 10:166–169PubMedGoogle Scholar
  70. Rahmann H, Slenzka, K, Anken RH et al. (1995) Structure- and function-related neuronal plasticity of the CNS of aquatic vertebrates during early ontogenetic development under microgravity conditions. In: Sahm P (ed) Scientific results of the German Spacelab Mission D-2, Wissenschafliche Projektleitung D-2, Aachen, pp 621–637Google Scholar
  71. Rahmann H, Hilbig R, Flemming J et al (1996) Influence of long-term altered gravity on the swimming performance of developing cichlid fish: including results from the 2nd German Spacelab Mission D-2. Adv Space Res 17:121–124CrossRefPubMedGoogle Scholar
  72. Riley B, Moorman S (2000) Development of utricular otoliths, but not saccular otoliths, is necessary for vestibular function and survival in zebrafish. J Neurobiol 43:329–337CrossRefPubMedGoogle Scholar
  73. Riley B, Zhu C, Janetopoulos C et al (1997) A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish. Dev Biol 191:191–201CrossRefPubMedGoogle Scholar
  74. Rogers P, Lewis T (1995) Startle reflex in fish. J Acoust Soc Am 98:2939. https://doi.org/10.1121/1.414111 CrossRefGoogle Scholar
  75. Schick J (2007) Rasterelektronenmikroskopische Aspekte zur Genese der Otolithen bei Buntbarschen (Oreochromis mossambiccus). State examination thesis, Institute of Zoology, University of Hohenheim, StuttgartGoogle Scholar
  76. Schulz-Mirbach T, Ladich F, Plath M et al (2014) Accessory hearing structures linked to inner ear morphology? Insights from 3D orientation patterns of ciliary bundles in three cichlid species. Front Zool 11:article 25. https://doi.org/10.1186/1742-9994-11-25 CrossRefGoogle Scholar
  77. Sebastian C, Esseling K, Horn E (2001) Altered gravitational forces affect the development of the static vestibuloocular reflex in fish (Oreochromis mossambicus). J Neurobiol 46:59–72CrossRefPubMedGoogle Scholar
  78. Simmler M, Zwaenepoel I, Verpy E et al (2000) Twister mutant mice are defective for otogelin, a component specific to inner ear acellular membranes. Mamm Genome 11:961–966CrossRefPubMedGoogle Scholar
  79. Söllner C, Nicolson T (2005) The zebrafish as a genetic model to study otolith formation. In: Bäuerlein E (ed) Biomineralization: progress in biology, molecular biology and application, 2nd edn. Wiley VCH, Weinheim, pp 229–242CrossRefGoogle Scholar
  80. Söllner C, Burghammer M, Busch-Nentwich E et al (2003) Control of crystal size and lattice formation by starmaker in otolith biomineralization. Science 302:282–286CrossRefPubMedGoogle Scholar
  81. Stooke-Vaughan G, Huang P, Hammond K et al (2012) The role of hair cells, cilia and ciliary motility in otolith formation in the zebrafish otic vesicle. Development 139:1777–1787CrossRefPubMedPubMedCentralGoogle Scholar
  82. Strauch S, Schuster M, Lebert M et al (2008) A closed ecological system in a space experiment. In: Proceedings of the symposium on life in space for life on earth, ESA-SP 553, id.41Google Scholar
  83. Takabayashi A, Ohara K, Ohmura T et al (1998) Mechanism of vestibular adaptation of fish under microgravity. Biol Sci Space 11:351–354CrossRefGoogle Scholar
  84. Takabayashi A, Iwata K, Ohmura-Iwasaki T et al (2004) Vestibulo-ocular reflex and gravity in fish. Biol Sci Space 18:132–133PubMedGoogle Scholar
  85. Thalmann I, Hughes I, Tong B et al (2006) Microscale analysis of proteins in inner ear tissues and fluids with emphasis on endolymphatic sac, otoconia, and organ of Corti. Electrophoresis 27:1598–1608. https://doi.org/10.1002/elps.200500768 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Tohse H, Mugiya Y (2001) Effects of enzyme and anion transport inhibitors on in vitro incorporation of inorganic carbon and calcium into endo-lymph and otoliths in salmon Oncorhynchus masou. Comp Biochem Physiol A 128:177–184CrossRefGoogle Scholar
  87. van Loon J (2016) Centrifuges for microgravity simulation. The reduced gravity paradigm. Front AstronSpace Sci 3:article 21. https://doi.org/10.3389/fspas.2016.00021 Google Scholar
  88. von Baumgarten R (1986) European vestibular experiments on the Spacelab-1 mission: 1. Overview. Exp Brain Res 64:239–246CrossRefGoogle Scholar
  89. von Baumgarten R, Thümler R (1979) A model for vestibular function in altered gravitational states. Life Sci Space Res 17:161–170CrossRefGoogle Scholar
  90. von Baumgarten R, Baldrighi G, Atema J et al (1970) Behavioral responses to linear accelerations in blind goldfish. Space Life Sci 3:25–33Google Scholar
  91. von Baumgarten R, Baldrighi G, Schillinger G (1972) Vestibular behaviour in fish during diminished G-force and weightlessness. Aerospace Med 43:626–632Google Scholar
  92. von Holst E (1935) Über den Lichtrückenreflex bei Fischen. Publ Zool Stat Napoli 15:143–158Google Scholar
  93. von Holst E (1950) Die Arbeitsweise des Statolithenapparates bei Fischen. Z vergl Physiol 33:60–120CrossRefGoogle Scholar
  94. Wada H, Dambly-Chaudière C, Kawakami K et al (2013) Innervation is required for sense organ development in the lateral line system of adult zebrafish. Proc Natl Acad Sci U S A 110:5659–5664. https://doi.org/10.1073/pnas.1214004110 PMCID: PMC3619376 Neuroscience CrossRefPubMedPubMedCentralGoogle Scholar
  95. Watanabe S, Takabayashi A, Takagi S et al (1989) Dorsal light response and changes of its responses under varying acceleration conditions. Adv Space Res 9:231–240CrossRefPubMedGoogle Scholar
  96. Watanabe S, Takabayashi A, Tanaka M et al (1991) Neurovestibular physiology in fish. Adv Space Biol Med 1:99–128CrossRefPubMedGoogle Scholar
  97. Weigele J, Franz-Odendaal T, Hilbig R (2015a) Spatial expression of otolith matrix protein-1 and Otolin-1 in normally and kinetotically swimming fish. Anat Rec 298:1765–1773CrossRefGoogle Scholar
  98. Weigele J, Franz-Odendaal T, Hilbig R (2015b) Expression of SPARC and the Osteopontin-like protein during skeletal development in the cichlid fish Oreochromis mossambicus. Dev Dyn 244:955–972. https://doi.org/10.1002/DVDY.24293 CrossRefPubMedGoogle Scholar
  99. Weigele J, Franz-Odendaal T, Hilbig R (2016) Formation of the inner ear during embryonic and larval development of the cichlid fish (Oreochromis mossambicus). Connect Tissue Res 58:172–195. https://doi.org/10.1080/03008207.2016.1198337 CrossRefPubMedGoogle Scholar
  100. Wiederhold M, Harrison J, Gao W (2000) Otoliths developed in microgravity. J Gravit Physiol 7:39–42Google Scholar
  101. Wiederhold M, Harrison J, Gao W (2003) A critical period for gravitational effects on otolith formation. J Vest Res 13:205–214Google Scholar
  102. Yan H, Popper A (1993) Acoustic intensity discrimination by the cichlid fish Astronotus ocellatus (Cuvier). J Comp Physiol A 173:347–351CrossRefPubMedGoogle Scholar
  103. Yanagihara D, Watanabe S, Takagi S et al (1993) Neuroanatomical substrate for the dorsal light response. II. Effects of kainic acid-induced lesions of the valvula cerebelli on the goldfish dorsal light response. Neurosci Res 16:33–37CrossRefPubMedGoogle Scholar

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© The Author(s) 2017

Authors and Affiliations

  1. 1.Institute of ZoologyUniversity of HohenheimStuttgartGermany
  2. 2.German Aerospace CentreInstitute of Aerospace Medicine, Gravitational BiologyCologneGermany

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