SpringerLink
Log in

Increase in telencephalic dopamine and cerebellar norepinephrine contents by hydrostatic pressure in goldfish: the possible involvement in hydrostatic pressure-related locomotion

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Fish are faced with a wide range of hydrostatic pressure (HP) in their natural habitats. Additionally, freshwater fish are occasionally exposed to rapid changes in HP due to heavy rainfall, flood and/or dam release. Accordingly, variations in HP are one of the most important environmental cues for fish. However, little information is available on how HP information is perceived and transmitted in the central nervous system of fish. The present study examined the effect of HP (water depth of 1.3 m) on the quantities of monoamines and their metabolites in the telencephalon, optic tectum, diencephalon, cerebellum (including partial mesencephalon) and vagal lobe (including medulla oblongata) of the goldfish, Carassius auratus, using high-performance liquid chromatography. HP affected monoamine and metabolite contents in restricted brain regions, including the telencephalon, cerebellum and vagal lobe. In particular, HP significantly increased the levels of dopamine (DA) in the telencephalon at 15 min and that of norepinephrine (NE) in the cerebellum at 30 min. In addition, HP also significantly increased locomotor activity at 15 and 30 min after HP treatment. It is possible that HP indirectly induces locomotion in goldfish via telencephalic DA and cerebellar NE neuronal activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Atema J (1971) Structures and functions of the sense of taste in the catfish (Ictalurus natalis). Brain Behav Evol 4:273–294

    Article  CAS  PubMed  Google Scholar 

  • Block BA, Booth D, Carey FG (1992) Direct measurement of swimming speeds and depth of blue marlin. J Exp Biol 166:267–284

    Google Scholar 

  • Bonn U (1987) Distribution of monoamine-containing neurons in the brain of a teleost, Carassius auratus (Cyprinidae). J Hirnforsch 28:529–544

    CAS  PubMed  Google Scholar 

  • Contestabile A, Villani L, Bissoli R, Poli A, Migani P (1986) Cholinergic, GABAergic and excitatory amino acidic neurotransmission in the goldfish vagal lobe. Exp Brain Res 63:301–309

    Article  CAS  PubMed  Google Scholar 

  • Corio M, Peute J, Steinbusch HWM (1991) Distribution of serotonin- and dopamine-immunoreactivity in the brain of the teleost Clarias gariepinus. J Chem Neuroanat 4:79–95

    Article  CAS  PubMed  Google Scholar 

  • Damasceno-Oliveira A, Fernández-Durán B, Gonçalves J, Serrão P, Soares-Da-Silva P, Reis-Henriques MA, Coimbra J (2006) Effects of cyclic and constant hydrostatic pressure on norepinephrine and epinephrine levels in the brain of flounder. J Fish Biol 68:1300–1307

    Article  Google Scholar 

  • Damasceno-Oliveira A, Fernandez-Duran B, Goncalves J, Serrao P, Soares-da-Silva P, Reis-Henriques MA, Coimbra J (2007) Effects of cyclic hydrostatic pressure on the brain biogenic amines concentrations in the flounder, Platichthys flesus. Gen Comp Endocrinol 153:385–389

    Article  CAS  PubMed  Google Scholar 

  • De Pedro N, Pinillos ML, Valenciano AI, Alonso-Bedate M, Delgado MJ (1998) Inhibitory effect of serotonin on feeding behavior in goldfish: involvement of CRF. Peptides 19:505–511

    Article  PubMed  Google Scholar 

  • Dietrich M, Hofmann MH, Bleckmann H (2002) Effects of dopaminergic drugs and telencephalic ablation on eye movements in the goldfish, Carassius auratus. Brain Res Bull 57:393–395

    Article  CAS  PubMed  Google Scholar 

  • Fenwick JC (1970) Brain serotonin and swimming activity in the goldfish, Carassius auratus. Comp Biochem Physiol 32:803–806

    Article  CAS  Google Scholar 

  • Finger TE (2008) Sorting food from stones: the vagal taste system in goldfish, Carassius auratus. J Comp Physiol A 194:135–143

    Article  Google Scholar 

  • Fraser PJ, Macdonald AG (1994) Crab hydrostatic pressure sensors. Nature 371:383–384

    Article  Google Scholar 

  • Fraser PJ, Shelmerdine RL (2002) Dogfish hair cells sense hydrostatic pressure. Nature 415:495–496

    Article  CAS  PubMed  Google Scholar 

  • Fraser PJ, Cruickshank SF, Shelmerdine RL (2003) Hydrostatic pressure effects on vestibular hair cell afferents in fish and crustacea. J Vestib Res 13:235–242

    PubMed  Google Scholar 

  • Fremberg M, van Veen T, Hartwig HG (1977) Formaldehyde-induced fluorescence in the telencephalon and diencephalon of the eel (Anguilla anguilla l.). A fluorescence-microscopic and microspectrofluorometric investigation with special reference to the innervation of the pituitary. Cell Tissue Res 176:1–22

    Article  CAS  PubMed  Google Scholar 

  • Gardette R, Krupa M, Crepel F (1987) Differential effects of serotonin on the spontaneous discharge and on the excitatory amino acid-induced responses of deep cerebellar nuclei neurons in rat cerebellar slices. Neuroscience 23:491–500

    Article  CAS  PubMed  Google Scholar 

  • Geffard M, Kah O, Onteniente B, Seguela P, Le Moal M, Delaage M (1984) Antibodies to dopamine: radioimmunological study of specificity in relation to immunocytochemistry. J Neurochem 42:1593–1599

    Article  CAS  PubMed  Google Scholar 

  • Gibson RN (1970) The tidal rhythm of activity of Coryphoblennius galerita (L.) (Teleostei, Blenniidae). Anim Behav 18:539–543

    Article  Google Scholar 

  • Gibson RN (1984) Hydrostatic pressure and the rhythmic behaviour of intertidal marine fishes. Trans Am Fish Soc 113:479–483

    Article  Google Scholar 

  • Gibson RN (1992) Tidally-synchronised behaviour in marine fishes. In: Ali MA (ed) Rhythms in fishes. Springer, New York, pp 63–81

    Chapter  Google Scholar 

  • Gnegy ME (2012) Catecholamine. In: Brady ST, Siegel GJ, Albers RW, Price DL (eds) Basic neurochemistry: Principles of molecular, cellular, and medical neurobiology. Elsevier Academic Press, Amsterdam, pp 283–293

    Chapter  Google Scholar 

  • Godø OR, Michalsen K (2000) Migratory behaviour of north-east Arctic cod, studied by use of data storage tags. Fish Res 48:127–140

    Article  Google Scholar 

  • Go** G, Pollard HB, Adeyemo OM, Kuijpers GA (1995) Effect of MPTP on dopaminergic neurons in the goldfish brain: a light and electron microscope study. Brain Res 687:35–52

    Article  CAS  PubMed  Google Scholar 

  • Gotow T, Triller A, Korn H (1990) Differential distribution of serotoninergic inputs on the goldfish Mauthner cell. J Comp Neurol 292:255–268

    Article  CAS  PubMed  Google Scholar 

  • Hensler JG (2012) Serotonin. In: Brady ST, Siegel GJ, Albers RW, Price DL (eds) Basic neurochemistry: Principles of molecular, cellular, and medical neurobiology. Elsevier Academic Press, Amsterdam, pp 300–322

    Chapter  Google Scholar 

  • Hornby PJ, Piekut DT (1990) Distribution of catecholamine-synthesizing enzymes in goldfish brains: presumptive dopamine and norepinephrine neuronal organization. Brain Behav Evol 35:49–64

    Article  CAS  PubMed  Google Scholar 

  • Ikenaga T, Yoshida M, Uematsu K (2005) Morphology and immunohistochemistry of efferent neurons of the goldfish corpus cerebelli. J Comp Neurol 487:300–311

    Article  CAS  PubMed  Google Scholar 

  • Ikenaga T, Yoshida M, Uematsu K (2006) Cerebellar efferent neurons in teleost fish. Cerebellum 5:268–274

    Article  CAS  PubMed  Google Scholar 

  • Janssen J, Brandt SB (1980) Feeding ecology and vertical migration of adult alewives (Alosa pseudoharengus) in lake Michigan. Can J Fish Aquat Sci 37:177–184

    Article  Google Scholar 

  • Kah O, Chambolle P (1983) Serotonin in the brain of the goldfish, Carassius auratus. An immunocytochemical study. Cell Tissue Res 234:319–333

    Article  CAS  PubMed  Google Scholar 

  • Kapsimali M, Vidal B, Gonzalez A, Dufour S, Vernier P (2000) Distribution of the mRNA encoding the four dopamine D1 receptor subtypes in the brain of the european eel (Anguilla anguilla): comparative approach to the function of D1 receptors in vertebrates. J Comp Neurol 419:320–343

    Article  CAS  PubMed  Google Scholar 

  • Koizumi I, Kanazawa Y, Tanaka Y (2013) The fishermen were right: experimental evidence for tributary refuge hypothesis during floods. Zool Sci 30:375–379

    Article  PubMed  Google Scholar 

  • Lee M, Strahlendorf JC, Strahlendorf HK (1985) Modulatory action of serotonin on glutamate-induced excitation of cerebellar purkinje cells. Brain Res 361:107–113

    Article  CAS  PubMed  Google Scholar 

  • Lillesaar C (2011) The serotonergic system in fish. J Chem Neuroanat 41:294–308

    Article  CAS  PubMed  Google Scholar 

  • Linard B, Bennani S, Jego P, Saligaut C (1996) Tyrosine hydroxylase activity and dopamine turnover of rainbow trout (Oncorhynchus mykiss) brain: the special status of the hypothalamus. Fish Physiol Biochem 15:41–48

    Article  CAS  PubMed  Google Scholar 

  • Macdonald AG, Gilchrist I, Wardle CS (1987) Effect of hydrostatic pressure on the motor activity of fish from shallow water and 900 m depths: some results of challenger cruise 6B/85. Comp Biochem Physiol 88:543–547

    Article  CAS  Google Scholar 

  • Matsumoto N, Yoshida M, Uematsu K (2007) Effects of partial ablation of the cerebellum on sustained swimming in goldfish. Brain Behav Evol 70:105–114

    Article  PubMed  Google Scholar 

  • McCleave JD, Arnold GP (1999) Movements of yellow- and silver-phase European eels (Anguilla anguilla L.) tracked in the western North Sea. ICES J Mar Sci 56:510–536

    Article  Google Scholar 

  • Mok EY, Munro AD (1998) Effects of dopaminergic drugs on locomotor activity in teleost fish of the genus Oreochromis (Cichlidae): involvement of the telencephalon. Physiol Behav 64:227–234

    Article  CAS  PubMed  Google Scholar 

  • Morita Y, Ito H, Masai H (1980) Central gustatory paths in the crucian carp, Carassius carassius. J Comp Neurol 191:119–132

    Article  CAS  PubMed  Google Scholar 

  • Nilsson GE (1989) Regional distribution of monoamines and monoamine metabolites in the brain of the crucian carp (Carassius carassius L.). Comp Biochem Physiol C 94:223–228

    Article  Google Scholar 

  • Nishi K, Kondo T, Narabayashi H (1991) Destruction of norepinephrine terminals in 1-metyl-4phenyl-1,2,3,6-tetrahydropyridine (MPTP)-treated mice reduces locomotor activity induced by L-DOPA. Neurosci Lett 123:244–247

    Article  CAS  PubMed  Google Scholar 

  • Northcott SJ (1991) A comparison of circatidal rhythmicity and entrainment by hydrostatic pressure cycles in the rock goby, Gobius paganellus L. and the shanny, Lipophrys pholis (L.). J Fish Biol 39:25–33

    Article  Google Scholar 

  • Northcott SJ, Gibson RN, Morgan E (1991a) Phase responsiveness of the activity rhythm of Lipophrys pholis (L.) (Teleostei) to a hydrostatic pressure pulse. J Exp Mar Biol Ecol 148:47–57

    Article  Google Scholar 

  • Northcott SJ, Gibson RN, Morgan E (1991b) The effect of tidal cycles of hydrostatic pressure on the activity of Lipophrys pholis (L.) (Teleostei). J Exp Mar Biol Ecol 148:35–45

    Article  Google Scholar 

  • Nunn AD, Copp GH, Vilizzi L, Carter MG (2010) Seasonal and diel patterns in the migrations of fishes between a river and a floodplain tributary. Ecol Freshw Fish 19:153–162

    Article  Google Scholar 

  • Olcese JM, Hall TR, Figueroa HR, de Vlaming VL (1979) Hypothalamic monoamine oxidase, a component in the serotonergic control of pituitary prolactin content in Carassius auratus L. Gen Comp Endocrinol 38:309–313

    Article  CAS  PubMed  Google Scholar 

  • Pollard HB, Dhariwal K, Adeyemo OM, Markey CJ, Caohuy H, Levine M, Markey S, Youdim MB (1992) A parkinsonian syndrome induced in the goldfish by the neurotoxin MPTP. FASEB J 6:3108–3116

    CAS  PubMed  Google Scholar 

  • Pollard HB, Kuijpers GA, Adeyemo OM, Youdim MB, Go** G (1996) The MPTP-induced parkinsonian syndrome in the goldfish is associated with major cell destruction in the forebrain and subtle changes in the optic tectum. Exp Neurol 142:170–178

    Article  CAS  PubMed  Google Scholar 

  • Raffaelli D, Richner H, Summers R, Northcott S (1990) Tidal migrations in the flounder (Platichthys flesus). Mar Behav Physiol 16:249–260

    Article  Google Scholar 

  • Roberts BL, van Rossem A, de Jager S (1992) The influence of cerebellar lesions on the swimming performance of the trout. J Exp Biol 167:171–178

    CAS  PubMed  Google Scholar 

  • Sebert P, Barthelemy L, Caroff J (1985) Serotonin levels in fish brain: effects of hydrostatic pressure and water temperature. Experientia 41:1429–1430

    Article  CAS  Google Scholar 

  • Sebert P, Barthelemy L, Caroff J (1986) Catecholamine content (as measured by the HPLC method) in brain and blood plasma of the EEL: effects of 101 ATA hydrostatic pressure. Comp Biochem Physiol C 84:155–157

    Article  CAS  PubMed  Google Scholar 

  • Sébert ME, Weltzien FA, Moisan C, Pasqualini C, Dufour S (2008) Dopaminergic systems in the European eel: characterization, brain distribution, and potential role in migration and reproduction. In: Dufour S, Prévost E, Rochard E, Williot P (eds) Fish and diadromy in Europe (ecology, management, conservation). Springer, Netherlands, pp 27–46

    Chapter  Google Scholar 

  • Somoza GM, Peter RE (1991) Effects of serotonin on gonadotropin and growth hormone release from in vitro perifused goldfish pituitary fragments. Gen Comp Endocrinol 82:103–110

    Article  CAS  PubMed  Google Scholar 

  • Strahlendorf JC, Lee M, Strahlendorf HK (1989) Modulatory role of serotonin on GABA-elicited inhibition of cerebellar Purkinje cells. Neuroscience 30:117–125

    Article  CAS  PubMed  Google Scholar 

  • Takemura A, Uchimura M, Shibata Y (2010a) Dopaminergic activity in the brain of a tropical wrasse in response to changes in light and hydrostatic pressure. Gen Comp Endocrinol 166:513–519

    Article  CAS  PubMed  Google Scholar 

  • Takemura A, Rahman MS, Park YJ (2010b) External and internal controls of lunar-related reproductive rhythms in fishes. J Fish Biol 76:7–26

    Article  CAS  PubMed  Google Scholar 

  • Takemura A, Shibata Y, Takeuchi Y, Hur SP, Sugama N, Badruzzaman M (2012) Effects of hydrostatic pressure on monoaminergic activity in the brain of a tropical wrasse, Halicoeres trimaculatus: possible implication for controlling tidal-related reproductive activity. Gen Comp Endocrinol 175:173–179

    Article  CAS  PubMed  Google Scholar 

  • Tanaka H, Naito Y, Davis ND, Urawa S, Ueda H, Fukuwaka M (2005) First record of the at-sea swimming speed of a Pacific salmon during its oceanic migration. Mar Ecol Prog Ser 291:307–312

    Article  Google Scholar 

  • Thompson RH, Menard A, Pombal M, Grillner S (2008) Forebrain dopamine depletion impairs motor behavior in lamprey. Euro J Neurosci 27:1452–1460

    Article  CAS  Google Scholar 

  • Vetillard A, Benanni S, Saligaut C, Jego P, Bailhache T (2002) Localization of tyrosine hydroxylase and its messenger RNA in the brain of rainbow trout by immunocytochemistry and in situ hybridization. J Comp Neurol 449:374–389

    Article  CAS  PubMed  Google Scholar 

  • Vidal B, Pasqualini C, Le Belle N, Holland MC, Sbaihi M, Vernier P, Zohar Y, Dufour S (2004) Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European EEL: a neuroendocrine lock for the onset of puberty. Biol Reprod 71:1491–1500

    Article  CAS  PubMed  Google Scholar 

  • Weinreb O, Youdim MB (2007) A model of MPTP-induced Parkinson’s disease in the goldfish. Nat Proto 2:3016–3021

    Article  CAS  Google Scholar 

  • Wollmuth LP, Crawshaw L, Panayiotides-Djaferis H (1989) The effects of dopamine on temperature regulation in goldfish. J Comp Physiol B 159:83–89

    Article  CAS  PubMed  Google Scholar 

  • Yoshida M, Nagatsu I, Kawakami-Kondo Y, Karasawa N, Spatz M, Nagatsu T (1983) Monoaminergic neurons in the brain of goldfish as observed by immunohistochemical techniques. Experientia 39:1171–1174

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Ms. Chihiro Yamauchi, University of the Ryukyus, and Dr. Yoriko Akimoto, Mr. Takahiro Nakashita, Mr. Seiya Mochinaga and Mr. Takeshi Yoshihara, Kyushu University, for their support and help in sampling. Dr. Sethu Selvaraj, Kyushu University, Dr. Takeshi Onuma, Osaka University, and Mr. Makoto Yoshida, The University of Tokyo, provided stimulating discussions and helpful advice. This study was supported by a Grant-in-Aid for JSPS fellows (Grant Numbers 10J02886 and 12J02083) to TI from the Japan Society for the Promotion of Science.

Author information

Author notes

  1. Taro Ikegami

    Present address: Department of Otorhinolaryngology, Head and Neck Surgery, Graduate School of Medicine, University of the Ryukyus, Nishihara, Okinawa, 903-0215, Japan

Authors and Affiliations

  1. Department of Chemistry, Biology, and Marine Science, Faculty of Science, University of the Ryukyus, Senbaru 1, Nishihara, Okinawa, 903-0213, Japan

    Taro Ikegami, Akihiro Takemura, Eunjung Choi & Muhammad Badruzzaman

  2. Laboratory of Regulation in Metabolism and Behavior, Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka, 812-8581, Japan

    Atsushi Suda & Mitsuhiro Furuse

  3. Laboratory of Nutritional Science for Animals, Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Shozo Tomonaga

Authors
  1. Taro Ikegami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akihiro Takemura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eunjung Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Atsushi Suda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shozo Tomonaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Muhammad Badruzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mitsuhiro Furuse
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Taro Ikegami.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ikegami, T., Takemura, A., Choi, E. et al. Increase in telencephalic dopamine and cerebellar norepinephrine contents by hydrostatic pressure in goldfish: the possible involvement in hydrostatic pressure-related locomotion. Fish Physiol Biochem 41, 1105–1115 (2015). https://doi.org/10.1007/s10695-015-0072-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-015-0072-7

Keywords

Search

Navigation