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Species-specific differences in sensorimotor adaptation are correlated with differences in social structure

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Abstract

Here, we report a species difference in the strength and duration of long-term sensorimotor adaptation in the electromotor output of weakly electric fish. The adaptation is produced by changes in intrinsic excitability in the electromotor pacemaker nucleus; this change is a form of memory that correlates with social structure. A weakly electric fish may be jammed by a similar electric organ discharge (EOD) frequency of another fish and prevents jamming by transiently raising its own emission frequency, a behavior called the jamming avoidance response (JAR). The JAR requires activation of NMDA receptors, and prolonged JAR performance results in long-term frequency elevation (LTFE) of a fish’s EOD frequency for many hours after the jamming stimulus. We find that LTFE is stronger in a shoaling species (Eigenmannia virescens) with a higher probability of encountering jamming conspecifics, when compared to a solitary species (Apteronotus leptorhynchus). Additionally, LTFE persists in Eigenmannia, whereas, it decays over 5–9 h in Apteronotus.

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Abbreviations

JAR:

Jamming avoidance response

EOD:

Electric organ discharge

LTFE:

Long-term frequency elevation

LTFD:

Long-term frequency depression

PMn:

Pacemaker nucleus

SPPn:

Sublemniscal prepacemaker nucleus

PPn-G:

Thalamic prepacemaker nucleus portion G

NMDA:

N-methyl-D-aspartatic acid

AMPA:

alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

References

  • Aizenman CD, Linden DJ (2000) Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 3:109–111

    Article  PubMed  CAS  Google Scholar 

  • Alkon DL (1984) Changes of membrane currents during learning. J Exp Biol 112:95–112

    PubMed  CAS  Google Scholar 

  • Bastian J (1987) Electrolocation in the presence of jamming signals: behavior. J Comp Physiol A 161:811–824

    Article  PubMed  CAS  Google Scholar 

  • Bennett MVL (1971) Electric organs. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic, New York, pp 493–574

    Google Scholar 

  • Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39

    Article  PubMed  CAS  Google Scholar 

  • Bullock TH (1993) How are more complex brains different? One view and an agenda for comparative neurobiology. Brain Behav Evol 41:88–96

    Article  PubMed  CAS  Google Scholar 

  • Bullock TH, Hamstra RH, Scheich H (1972a) The jamming avoidance response of high-frequency electric fish. I. General features. J Comp Physiol 77:1–22

    Article  Google Scholar 

  • Bullock TH, Hamstra RH, Scheich H (1972b) The jamming avoidance response of high frequency electric fish. II. Quantitative aspects. J Comp Physiol 77:23–48

    Article  Google Scholar 

  • Butefisch CM (2004) Plasticity in the human cerebral cortex: lessons from the normal brain and from stroke. Neuroscientist 10:163–173

    Article  PubMed  Google Scholar 

  • Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623–634

    Article  PubMed  CAS  Google Scholar 

  • Crampton WGR (1998) Electric signal design and habitat preferences in a species rich assemblage of gymnotiform fishes from the Upper Amazon basin. An Acad Bras Cienc 70:805–847

    Google Scholar 

  • Donoghue JP (1995) Plasticity of adult sensorimotor representations. Curr Opin Neurobiol 5:749–754

    Article  PubMed  CAS  Google Scholar 

  • Dunlap KD, Oliveri LM (2002) Retreat site selection and social organization in captive electric fish, Apteronotus leptorhynchus. J Comp Physiol A 188:469–477

    Article  CAS  Google Scholar 

  • Dye J (1988) An in vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish, Apteronotus. J Comp Physiol A 163:445–458

    Article  PubMed  CAS  Google Scholar 

  • Dye J, Heiligenberg W, Keller CH, Kawasaki M (1989) Different classes of glutamate receptors mediate distinct behaviors in a single brainstem nucleus. Proc Natl Acad Sci USA 86:8993–8997

    Article  PubMed  CAS  Google Scholar 

  • Fortune, ES, Tan, EW, Nizar, J (2003) Relation of group size to the control of electric organ discharges in gymnotiform fish. In: Abstract viewer/itinerary planner. Washington, DC: Society for Neuroscience, 2003. Online.

  • Gaddis P (1977) Communication by harmonization of electric organ discharge frequencies by Eigenmannia virescens (Sternopygidae, Pisces). Rev Can Biol 36:317–320

    PubMed  CAS  Google Scholar 

  • Hagedorn M, Heiligenberg W (1985) Court and spark: electric signals in the courtship and mating of gymnotoid fish. Anim Behav 33:254–265

    Article  Google Scholar 

  • Heiligenberg W (1991) Neural nets in electric fish. MIT Press. Cambridge

    Google Scholar 

  • Heiligenberg W (1973) Electrolocation of objects in the electric fish Eigenmannia (Rhamphichthyidae, Gymnotoidei). J Comp Physiol 87:137–164

    Article  Google Scholar 

  • Heiligenberg W, Metzner W, Wong CJ, Keller CH (1996) Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates. J Comp Physiol A 179:653–674

    Article  PubMed  CAS  Google Scholar 

  • Held R, Freedman SJ (1963) Plasticity in human sensorimotor control. Science 142:455–462

    Article  PubMed  CAS  Google Scholar 

  • Hopkins CD (1988) Neuroethology of electric communication. Annu Rev Neurosci 11:497–535

    Article  PubMed  CAS  Google Scholar 

  • Houde JF, Jordan MI (1998) Sensorimotor adaptation in speech production. Science 279:1213–1216

    Article  PubMed  CAS  Google Scholar 

  • Juranek J, Metzner W (1997) Cellular characterization of synaptic modulations of a neuronal oscillator in electric fish. J Comp Physiol A 181:393–414

    Article  Google Scholar 

  • Kandel ER, Schwartz JH, Jessell TH (2000) Principles of neural science. McGraw-Hill. New York

    Google Scholar 

  • Katz PS, Harris-Warrick RM (1999) The evolution of neuronal circuits underlying species-specific behavior. Curr Opin Neurobiol 9:628–633

    Article  PubMed  CAS  Google Scholar 

  • Keeley BL (1995) Large, slow changes in electric organ discharge associated with social context in Eigenmannia. In: Nervous systems and behaviour: proceedings of the 4th international congress of neuroethology. Georg Thieme Verlag, Stuttgart, p 415

  • Knudsen EI (1975) Spatial aspects of the electric fields generated by weakly electric fish. J Comp Physiol 99:103–118

    Article  Google Scholar 

  • Knudsen EI (2002) Instructed learning in the auditory localization pathway of the barn owl. Nature 417:322–328

    Article  PubMed  CAS  Google Scholar 

  • Kramer B, Kirschbaum F, Markl H (1981) Species specificity of electric organ discharges in a sympatric group of gymnotid fishes from Manaus (Amazonas). Sensory physiology of aquatic lower vertebrates. Akademiai Kiado, Pergamon, pp 195–219

    Google Scholar 

  • Lisberger SG (1988) The neural basis for learning of simple motor skills. Science 242:728–735

    Article  PubMed  CAS  Google Scholar 

  • Lissmann HW (1961) Ecological studies on gymnotids. In: Chagas C, Paes de Carvalho A (eds) Bioelectrogenesis. Elsevier, Amsterdam, pp 215–226

    Google Scholar 

  • Malenka RC, Nicoll RA (1999) Long-term potentiation—a decade of progress? Science 285:1870–1874

    Article  PubMed  CAS  Google Scholar 

  • Marder E, Abbott LF, Turrigiano GG, Liu Z, Golowasch J (1996) Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci USA 93:13481–13486

    Article  PubMed  CAS  Google Scholar 

  • Oestreich J, Zakon HH (2002) The long-term resetting of a brainstem pacemaker nucleus by synaptic input: a model for sensorimotor adaptation. J Neurosci 22:8287–8296

    PubMed  CAS  Google Scholar 

  • Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes. Chapman and Hall, London, pp 363–439

    Google Scholar 

  • Rothman SM, Olney JW (1995) Excitotoxicity and the NMDA receptor—still lethal after eight years. Trends Neurosci 18:57–58

    Article  PubMed  CAS  Google Scholar 

  • Schlaug G (2001) The brain of musicians. A model for functional and structural adaptation. Ann N Y Acad Sci 930:281–299

    Article  PubMed  CAS  Google Scholar 

  • Schwassmann HO (1978) Ecological aspects of electroreception. In: Ali M (ed) Sensory ecology. Plenum, New York, pp 521–533

    Google Scholar 

  • Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. PNAS 93:13515–13522

    Article  PubMed  CAS  Google Scholar 

  • Steinbach AB (1970) Diurnal movements and discharge characteristics of electric gymnotid fishes in the Rio Negro, Brazil. Biol Bull 138:200–210

    Article  PubMed  CAS  Google Scholar 

  • Striedter GF (1998) A comparative perspective on motor learning. Neurobiol Learn Mem 70:189–196

    Article  PubMed  CAS  Google Scholar 

  • Watanabe A, Takeda K (1963) The change of discharge frequency by AC stimulus in a weakly electric fish. J Exp Biol 40:57–66

    Google Scholar 

  • Westby GWM (1988) The ecology discharge diversity and predatory behavior of gymnotiform electric fish in the coastal streams of French Guiana. Behav Ecol Sociobiol 22:341–354

    Google Scholar 

  • Wright WG (2000) Neuronal and behavioral plasticity in evolution: experiments in a model lineage. Biosci 50:883–894

    Article  Google Scholar 

  • Zakon HH (1986) The electroreceptive periphery. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 103–156

    Google Scholar 

  • Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885–900

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Nikolai Dembrow, George Pollak, Wesley Thompson, and Frank Triefenbach for helpful comments. This work was supported by grant NIH MH56535 (to HZ). The experiments comply with the "Principles of animal care", publication No. 86–23, revised 1985 of the National Institute of Health.

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  1. Jörg Oestreich

    Present address: Department of Neurobiology, Harvard Medical School, 220 Longwood Ave, Boston, MA, 02115, USA

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  1. Section of Neurobiology, University of Texas at Austin, Austin, TX, 78712, USA

    Jörg Oestreich & Harold H. Zakon

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  1. Jörg Oestreich
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  2. Harold H. Zakon
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Correspondence to Jörg Oestreich.

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Oestreich, J., Zakon, H.H. Species-specific differences in sensorimotor adaptation are correlated with differences in social structure. J Comp Physiol A 191, 845–856 (2005). https://doi.org/10.1007/s00359-005-0006-4

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  • DOI: https://doi.org/10.1007/s00359-005-0006-4

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