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Temperature dependent plasticity of habituation in the crayfish

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Abstract

To determine the effects of thermal preconditioning on a simple form of learning and memory, habituation, we preconditioned crayfish with extreme temperatures and subsequently analysed their effects on mechanosensory input that evokes a response in the lateral giant interneurons, within the normal temperature range of the animal. We found that repetitive stimulation with a 1 s interstimulus interval led to habituation of the response the lateral giant in control animals at 22°C. Neither heat nor cold preconditioning had any effect on the probability of evoking a response in the lateral giant nor on the rate at which habituation occurred. With a 1 min interstimulus interval, however, the rate of habituation of the lateral giant in the heat-preconditioned group was less than either the control or cold-preconditioned animals. The effect of heat or cold pre-exposure was specific to the input to the lateral giant at control temperatures. For example, at 22°C prior heat and cold preconditioning had no effect on spontaneous reductor motor neurone activity. They did, however, provide thermoprotection at extreme temperatures, with the probability of spontaneous activity higher in the cold-preconditioned group at low temperatures but higher in the heat-preconditioned group at higher temperatures.

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Abbreviations

CS:

Cold shock

CSP:

Cold-shock protein

HS:

Heat shock

HSP:

Heat-shock protein

ISI:

Interstimulus interval

LG:

Lateral giant

mRNA:

Messenger ribonucleic acid

SEM:

Standard error of the mean

References

  • Al-Fageeh MB, Smales CM (2006) Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem J 397:247–259

    Article  PubMed  CAS  Google Scholar 

  • Ammon-Treiber S, Grecksch G, Angelidis C, Vezyraki P, Höllt V, Becker A (2008) Emotional and learning behaviour in mice overexpressing heat shock protein 70. Neurobiol Learn Mem 90:358–364

    Article  PubMed  CAS  Google Scholar 

  • Antonsen BL, Edwards DH (2007) Mechanisms of serotonergic facilitation at a command neuron. J Neurophysiol 98:3494–3504

    Article  PubMed  Google Scholar 

  • Araki M, Nagayama T (2003) Direct chemically mediated synaptic transmission from mechanosensory afferents contributes to habituation of crayfish lateral giant escape reaction. J Comp Physiol A 189:731–739

    Article  CAS  Google Scholar 

  • Araki M, Nagayama T, Sprayberry J (2005) Cyclic AMP mediates serotonin-induced synaptic enhancement of lateral giant interneuron of the crayfish. J Neurophysiol 94:2644–2652

    Article  PubMed  CAS  Google Scholar 

  • Araki M, Nagayama T (2005) Decrease in excitability of LG following habituation of the crayfish escape reaction. J Comp Physiol A 191:481–489

    Article  Google Scholar 

  • Barclay JW, Robertson RM (2001) Enhancement of short term synaptic plasticity by prior environmental stress. J Neurophysiol 85:1332–1335

    PubMed  CAS  Google Scholar 

  • Beaumont V, Zucker RS (2000) Enhancement of synaptic transmission by cyclic AMP modulation of presynaptic I h channels. Nat Neurosci 3:133–141

    Article  PubMed  CAS  Google Scholar 

  • Brown IR (2007) Heat shock proteins and protection. Ann NY Acad Sci 1113:147–158

    Article  PubMed  CAS  Google Scholar 

  • Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92:351–366

    Article  PubMed  CAS  Google Scholar 

  • Burrows M (1989) Effect of temperature on a central synapse between identified motor neurons in the locust. J Comp Physiol A 165:687–695

    Article  PubMed  CAS  Google Scholar 

  • Castellucci V, Pinsker H, Kupfermann I, Kandel ER (1970) Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167:1745–1748

    Article  PubMed  CAS  Google Scholar 

  • Cowan DF, Watson WH, Solow AR, Mountcastle AM (2007) Thermal histories of brooding lobsters, Homarus americanus, in the Gulf of Maine. Mar Biol 150:463–470

    Article  Google Scholar 

  • Gao T, Newton AC (2002) The turn motif is a phosphorylation switch that regulates the binding of Hsp70 to protein kinase C. J Biol Chem 277:31585–31592

    Article  PubMed  CAS  Google Scholar 

  • Ghirardi M, Braha O, Hochner B, Montarolo P, Kandel E, Dale N (1992) Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron 9:479–489

    Article  PubMed  CAS  Google Scholar 

  • Graumann PL, Marahiel MA (1998) A superfamily of proteins that contain the cold-shock domain. Trends Biochem Sci 23:286–290

    Article  PubMed  CAS  Google Scholar 

  • Hamilton JL, Edwards CR, Holt SR, Worden MK (2007) Temperature dependent modulation of lobster neuromuscular properties by serotonin. J Exp Biol 210:1025–1035

    Article  PubMed  CAS  Google Scholar 

  • Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858

    Article  PubMed  CAS  Google Scholar 

  • Heitler WJ, Edwards DH (1998) Effect of temperature on a voltage-sensitive electrical synapse in crayfish. J Exp Biol 201:503–513

    PubMed  CAS  Google Scholar 

  • Heitler WJ, Goodman CS, Rowell CHF (1977) The effects of temperature on the threshold of identified neurons in the locust. J Comp Physiol A 117:163–182

    Article  Google Scholar 

  • Hirano M, Rome LC (1984) Jumping performance of frogs (Rana pipiens) as a function of muscle temperature. J Exp Biol 108:429–439

    Google Scholar 

  • Hoffmann AA, Sørensen SG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Thermal Biol 28:175–216

    Article  Google Scholar 

  • Jensen AJ (1990) Growth of young migratory brown trout Salmo trutta correlated with water temperature in Norwegian rivers. J Animal Ecol 59:603–614

    Article  Google Scholar 

  • Jiang W, Hou Y, Inouye M (1997) CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J Biol Chem 272:196–202

    Article  PubMed  CAS  Google Scholar 

  • Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038

    Article  PubMed  CAS  Google Scholar 

  • Kandel ER (2009) The biology of memory: a forty-year perspective. J Neurosci 29:12748–12756

    Article  PubMed  CAS  Google Scholar 

  • Karunanithi S, Barclay JW, Robertson RM, Brown IR, Atwood HL (1999) Neuroprotection at Drosophila synapses conferred by prior heat shock. J Neurosci 19:4360–4369

    PubMed  CAS  Google Scholar 

  • Kelty JD, Noseworthy PA, Feder ME, Robertson RM, Ramirez JM (2002) Thermal preconditioning and heat-shock protein 72 preserve synaptic transmission during thermal stress. J Neurosci 22, RC193: 1−6

  • Kelty JD, Killian KA, Lee RE (1996) Cold shock and rapid cold-hardening of pharate adult flesh flies (Sarcophaga crassipalpis): effects on behaviour and neuromuscular function following eclosion. Physiol Entomol 21:283–288

    Article  Google Scholar 

  • Krasne FB, Wine JJ (1987) Evasion responses of the crayfish. In: Guthrie DM (ed) Aims and Methods in Neuroethology. Manchester University Press, Manchester, pp 10–45

    Google Scholar 

  • Lasek RJ, Gainer H, Barker JL (1977) Cell-to-cell transfer of glial proteins to the squid giant axon: the glia-neuron protein transfer hypothesis. J Cell Biol 74:501–523

    Article  PubMed  CAS  Google Scholar 

  • Lee SH, Taylor K, Krasne FB (2008) Reciprocal stimulation of decay between serotonergic facilitation and depression of synaptic transmission. J Neurophysiol 100:1113–1126

    Article  PubMed  Google Scholar 

  • Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  PubMed  CAS  Google Scholar 

  • Nagayama T, Takahata M, Hisada M (1983) Local spikeless interaction of motoneuron dendrites in the crayfish Procambarus clarkia Girard. J Comp Physiol A 152:335–345

    Article  Google Scholar 

  • Nagayama T, Takahata M, Hisada M (1984) Functional characteristics of local nonspiking interneurons as the premotor elements in crayfish. J Comp Physiol A 154:499–510

    Article  Google Scholar 

  • Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57–69

    Article  PubMed  CAS  Google Scholar 

  • Robertson RM (2004) Modulation of neural circuit operation by prior environmental stress. Intgr Comp Biol 44:21–27

    Article  Google Scholar 

  • Rochelle JM, Grossfeld RM, Bunting DL, Tytell M, Dwyer BE, Xue Z (1991) Stress protein synthesis by crayfish CNS tissue in vitro. Neurochem Res 16:533–542

    Article  PubMed  CAS  Google Scholar 

  • Sheller RA, Smyers ME, Grossfeld RM, Ballinger M, Bittner GD (1998) Heat-shock proteins in axoplasm: high constitutive levels and transfer of inducible isoforms from glia. J Comp Neurol 396:1–11

    Article  PubMed  CAS  Google Scholar 

  • Stich H-B, Lampert W (1984) Growth and reproduction of migrating and non-migrating Daphnia species under simulated food and temperature conditions of diurnal vertical migration. Oecologia 61:192–196

    Article  Google Scholar 

  • Teshiba T, Shamsian A, Yashar B, Yeh S-R, Edwards DH, Krasne FB (2001) Dual and opposing modulatory effects of serotonin on crayfish lateral giant escape command neurons. J Neurosci 21:4523–4529

    PubMed  CAS  Google Scholar 

  • Van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–432

    Google Scholar 

  • Wine JJ, Krasne FB, Chen L (1975) Habituation and inhibition of the crayfish lateral giant escape response. J Exp Biol 62:771–783

    PubMed  CAS  Google Scholar 

  • Wine JJ (1984) The structural basis of an innate behavioural pattern. J Exp Biol 112:283–319

    Google Scholar 

  • Wine JJ, Krasne FB (1972) The organization of escape behaviour in the crayfish. J Exp Biol 56:1–18

    PubMed  CAS  Google Scholar 

  • Wine JJ, Krasne FB (1982) The cellular organisation of crayfish escape behaviour. In: Bliss ED (ed) The Biology of Crustaceans. Academic Press, New York, pp 241–292

    Google Scholar 

  • Whyard S, Wyatt GR, Walker VK (1986) The heat shock response in Locusta migratoria. J Comp Physiol 156B:813–817

    Google Scholar 

  • Zucker RS (1972) Crayfish escape behavior and central synapses. II. Physiological mechanisms underlying behavioral habituation. J Neurophysiol 35:621–637

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was made possible by a Japan Society for the Promotion of Science Furusato Award (London) and a Japan Society for the Promotion of Science Invitation Fellowship to PLN, and an award from the Ministry of Science, Sport, Culture and Technology to TN.

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Yamagata University, 990-8560, Yamagata, Japan

    Toshiki Nagayama

  2. School of Biological Sciences, University of Southampton, B85/3055 Highfield Campus, Southampton, SO17 1BJ, UK

    Philip L. Newland

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  1. Toshiki Nagayama
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  2. Philip L. Newland
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Correspondence to Philip L. Newland.

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Nagayama, T., Newland, P.L. Temperature dependent plasticity of habituation in the crayfish. J Comp Physiol A 197, 1073–1081 (2011). https://doi.org/10.1007/s00359-011-0668-z

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  • DOI: https://doi.org/10.1007/s00359-011-0668-z

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