Skip to main content
SpringerLink
Log in

Neuronal correlates of the visually elicited escape response of the crab Chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

When confronted with predators, animals are forced to take crucial decisions such as the timing and manner of escape. In the case of the crab Chasmagnathus, cumulative evidence suggests that the escape response to a visual danger stimulus (VDS) can be accounted for by the response of a group of lobula giant (LG) neurons. To further investigate this hypothesis, we examined the relationship between behavioral and neuronal activities within a variety of experimental conditions that affected the level of escape. The intensity of the escape response to VDS was influenced by seasonal variations, changes in stimulus features, and whether the crab perceived stimuli monocularly or binocularly. These experimental conditions consistently affected the response of LG neurons in a way that closely matched the effects observed at the behavioral level. In other words, the intensity of the stimulus-elicited spike activity of LG neurons faithfully reflected the intensity of the escape response. These results support the idea that the LG neurons from the lobula of crabs are deeply involved in the decision for escaping from VDS.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alvarez-Buylla A, Kirn JR (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33:585–601

    Article  PubMed  CAS  Google Scholar 

  • Aréchiga H, Rodríguez-Sosa L (2002) Distributed circadian rhythmicity in the crustacean nervous system. In: Wiese K (Ed) The crustacean nervous system. Springer, Berlin, pp 113–122

    Google Scholar 

  • Aréchiga H, Wiersma AG (1969) Circadian rhythm of responsiveness in crayfish visual units. J Neurobiol 1:71–85

    Article  PubMed  Google Scholar 

  • Bachmann S, Martinez MM (1999) Feeding tactics of the american oystercatcher (Haematopus palliatus) on Mar Chiquita coastal lagoon, Argentina. Ornit Neurotr 10:81–84

    Google Scholar 

  • Berón de Astrada M, Sztarker J, Tomsic D (2001) Visual interneurons of the crab Chasmagnathus studied by intracellular recordings in vivo. J Comp Physiol A 187:37–44

    Article  Google Scholar 

  • Berón de Astrada M, Tomsic D (2002) Physiology and morphology of visual movement detector neurons in a crab (Decapoda: Brachyura). J Comp Physiol A 188:539–551

    Article  Google Scholar 

  • Cannicci S, Barelli C, Vannini M (2000) Homing in the swimming crab Thalamita crenata: a mechanism based on underwater landmark memory. Anim Behav 60:203–210

    Article  PubMed  Google Scholar 

  • D’Incao F, Ruffino ML, Silva KG (1988) In: Notas preliminares sobre a ecologia de Chasmagnathus granulata (Dana, 1851) na barra de Rio Grande (Decapoda, Grapsidea) resumos XV congressos Brasileiros de zoologia, Curitiva, p 93

  • Edwards DH, Heitler WJ, Krasne FB (1999) Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci 22:153–161

    Article  PubMed  CAS  Google Scholar 

  • Ewert JP (1980) Neuroethology: an introduction to the neurophysiological fundamentals of behavior. Springer

  • Ewert JP (1987) Neuroethology of the releasing mechanism: prey-catching behavior in toads. Behav Brain Sci 10:337–405

    Google Scholar 

  • Ewert JP (1997) Neural correlates of key stimulus and releasing mechanism: a case study and two concepts. Trends Neurosci 230:332–339

    Google Scholar 

  • Ewert JP, Siefert G (1974a) Neuronal correlates of seasonal changes in contrast-detection of pray catching behavior in toads (Bufo bufo L.). Vision Res 14:431–432

    Article  PubMed  CAS  Google Scholar 

  • Ewert JP, Siefert G (1974b) Seasonal change of contrast detection in the toad’s Bufo bufo (L.) visual system. J Comp Physiol A 94:177–186

    Article  Google Scholar 

  • Ewert JP, Borchers HW, Wietersheim A (1978) Question of prey feature detectors in the toad’s Bufo bufo (L.) visual system: a correlation analysis. J Comp Physiol A 126:43–47

    Article  Google Scholar 

  • Fleissner G, Fleissner G (2006) Endogenous control of visual adaptation in invertebrates. In: Warrant E, Nilson D-E (Eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 127–166

    Google Scholar 

  • Freudenthal R, Romano A (2000) Participation of Rel/NF-kappaB transcription factors in long-term memory in the crab Chasmagnathus. Brain Res 855:274–281

    Article  PubMed  CAS  Google Scholar 

  • Groves PM, Lee D, Thompson RF (1969) Effects of stimulus frequency and intensity on habituation and sensitization in acute spinal cat. Physiol Behav 4:383–388

    Article  Google Scholar 

  • Hemmi JM, Zeil J (2003) Robust judgment of inter-object distance by an arthropod. Nature 421:160–163

    Article  PubMed  CAS  Google Scholar 

  • Hemmi JM (2005) Predator avoidance in fiddler crabs: 1. Escape decisions in relation to the risk of predation. Anim Behav 69:603–614

    Article  Google Scholar 

  • Hermitte G, Aggio J, Maldonado H (1995) Failure of interocular transfer in two types of learning in the crab Chasmagnathus. J Comp Physiol A 177:371–378

    Article  Google Scholar 

  • Jennions MD, Backwell PR, Murai M, Christy JH (2003) Hiding behavior in fiddler crabs: how long should prey hide in response to a potential predator? Anim Behav 66:251–257

    Article  Google Scholar 

  • Johnson AP, Horseman BG, Macauley MW, Barnes WJ (2002) PC-based visual stimuli for behavioural and electrophysiological studies of optic flow field detection. J Neurosci Methods 114:51–61

    Article  PubMed  Google Scholar 

  • Korn H, Faber DS (2005) The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47:13–28

    Article  PubMed  CAS  Google Scholar 

  • Kucharski LCR, Da Silva RSM (1991) Effect of diet composition on carbohydrate and lipid metabolism in an estuarian crab, C. granulata (Dana, 1851). Comp Biochem Physiol 99:215–218

    Article  Google Scholar 

  • Land MF, Layne J (1995a) The visual control of behaviour in fiddler crabs: I. Resolution, thresholds and the role of the horizon. J Comp Physiol A 177:81–90

    Article  Google Scholar 

  • Land MF, Layne J (1995b) The visual control of behavior in fiddler crabs: II. Tracking control systems in courtship and defense. J Comp Physiol A 177:91–103

    Google Scholar 

  • Layne J, Land M, Zeil J (1997) Fiddler crabs use the visual horizon to distinguish predators from conspecifics: a review of the evidence. J Mar Biol Ass UK 77:43–54

    Google Scholar 

  • Lozada M, Romano A, Maldonado H (1990) Long term habituation to a danger stimulus in the crab Chasmagnathus granulatus. Phys Behav 47:35–41

    Article  CAS  Google Scholar 

  • Medan V, Oliva D, Tomsic D (2007) Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus. J Neurophysiol 98:2414–2428

    Article  PubMed  Google Scholar 

  • Merlo E, Romano A (2007) Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus. Neurosci 147:46–52

    Article  CAS  Google Scholar 

  • Nalbach HO (1990) Discontinuous turning reaction during escape in soldier crabs. J Exp Biol 148:483–487

    Google Scholar 

  • Nottebohm F (1989) From bird song to neurogenesis. Sci Am 260:74–79

    PubMed  CAS  Google Scholar 

  • Oliva D, Medan V, Tomsic D (2007) Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae). J Exp Biol 210:865–880

    Article  PubMed  Google Scholar 

  • Pedreira ME, Maldonado H (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863–869

    Article  PubMed  CAS  Google Scholar 

  • Pedreira ME, Pérez-Cuesta L, Maldonado H (2002) Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: protein synthesis requirement and mediation by NMDA-type glutamatergic receptors. J Neurosci 22:8305–8311

    PubMed  CAS  Google Scholar 

  • Pedreira ME, Pérez-Cuesta L, Maldonado H (2004) Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn Mem 11:579–585

    Article  PubMed  Google Scholar 

  • Pereyra P, González Portino E, Maldonado H (2000) Long-lasting and context-specific freezing preference is acquired after spaced repeated presentations of a danger stimulus in the crab Chasmagnathus. Neurobiol Learn Mem 74:119–134

    Article  PubMed  CAS  Google Scholar 

  • Pereyra P, Saraco M, Maldonado H (1999) Decreased response or alternative defensive strategies in escape: two different types of long-term memory in the crab Chasmagnathus. J Comp Physiol A 184:301–310

    Article  Google Scholar 

  • Rakitin A, Tomsic D, Maldonado H (1991) Habituation and sensitization to an electrical shock in the crab Chasmagnathus. Effect of background illumination. Phys Behav 50:477–487

    Article  CAS  Google Scholar 

  • Rodríguez-Sosa L, De la Vega MT, Vergara P, Aréchiga H (1997) Seasonal rhythm of red pigment-concentrating hormone in the crayfish. Chronobiol Int 14:639–645

    PubMed  Google Scholar 

  • Rosas C, Sanchez A, Escobar E, Soto L, Bolongaro-Crevenna A (1992) Daily variations of oxygen consumption and glucose hemolymph level related to morphophysiological and ecological adaptations of crustacea. Comp Biochem Physiol 101:323–328

    Article  Google Scholar 

  • Santer RD, Rind FC, Stafford R, Simmons PJ (2006) Role of an identified looming-sensitive neuron in triggering a flying locust’s escape. J Neurophysiol 95:3391–3400

    Article  PubMed  Google Scholar 

  • Simmons P, Young D (1999) Nerve cells and animal behavior, (2nd Ed). Cambridge University Press

  • Strausfeld NJ (2005) Evolution of crustacean optic lobes and origins of chiasmata. Arthropod Struct Dev 34:235–56

    Article  Google Scholar 

  • Sztarker J (2000) Interneuronas monoculares y binoculares: indicios funcionales de la organización circuital del sistema visual en el cangrejo Chasmagnathus. Licenciate thesis, Universidad de Buenos Aires

  • Sztarker J, Strausfeld NJ, Tomsic D (2005) Organization of optic lobes that support motion detection in a semiterrestrial crab. J Comp Neurol 493:396–411

    Article  PubMed  Google Scholar 

  • Sztarker J, Tomsic D (2004) Binocular visual integration in the crustacean nervous system. J Comp Physiol A 190:951–962

    Google Scholar 

  • Thompson RF, Spencer WA (1966) Habituation: a model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73:16–43

    Article  PubMed  CAS  Google Scholar 

  • Tinbergen N (1951) The study of instinct. Clarendon Press, Oxford

    Google Scholar 

  • Tinbergen N, Perdeck AC (1950) On the stimulus situation releasing the begging responses in the newly hatched Herring Gull chick (Larus argentatus Pont.). Behaviour 3:1–38

    Article  Google Scholar 

  • Tomsic D (2002) Visual learning in crabs investigated by intracellular recordings in vivo. In: Wiese K (ed) The crustacean nervous system. Springer, Berlin, pp 328–335

    Google Scholar 

  • Tomsic D, Berón de Astrada M, Sztarker J (2003) Identification of individual neurons reflecting short- and long-term visual memory in an arthropod. J Neurosci 23:8539–8546

    PubMed  CAS  Google Scholar 

  • Tomsic D, Massoni V, Maldonado H (1993) Habituation to a danger stimulus in two semiterrestrial crabs. Ontogenic, ecological and opioid system correlates. J Comp Physiol A 173:621–633

    Article  Google Scholar 

  • Tomsic D, Pedreira ME, Romano A, Hermitte G, Maldonado H (1998) Context-US association as a determinant of long-term habituation in the crab Chasmagnathus. Ani Learn Behav 26:196–209

    Google Scholar 

  • Zeil J, Hemmi JM (2006) The visual ecology of fiddler crabs. J Comp Physiol A 192:1–25

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank John Tuthill for corrections to this manuscript. This work was supported by postdoctoral fellowships from the National Research Council of Argentina (CONICET) to J.S. and from the following research grants to D.T.: Universidad de Buenos Aires, grant number X 173; ANPCYT, grant number PICT 12300/02.

Author information

Authors and Affiliations

  1. Laboratorio de Neurobiología de la Memoria, Depto. Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires. IFIBYNE-CONICET, Pabellón 2 Ciudad Universitaria, 1428 , Buenos Aires, Argentina

    Julieta Sztarker & Daniel Tomsic

Authors
  1. Julieta Sztarker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Tomsic
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel Tomsic.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sztarker, J., Tomsic, D. Neuronal correlates of the visually elicited escape response of the crab Chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations. J Comp Physiol A 194, 587–596 (2008). https://doi.org/10.1007/s00359-008-0333-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-008-0333-3

Keywords

Search

Navigation