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Insect Hearing and Acoustic Communication pp 123–141Cite as

Towards an Understanding of the Neural Basis of Acoustic Communication in Crickets

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Part of the book series: Animal Signals and Communication ((ANISIGCOM,volume 1))

Abstract

Their conspicuous acoustic communication behaviour makes crickets excellent model systems to study the neural mechanisms underlying signal generation and auditory pattern recognition. Male singing is driven by a central pattern generator (CPG) housed in the metathoracic and anterior abdominal ganglia with rhythmically active opener and closer interneurons that can reset the chirp rhythm. Command neurons descending from the brain control the singing behaviour. Female phonotaxis is tuned towards the species-specific pattern of the male calling song and auditory orientation behaviour demonstrates a parallel organisation of pattern recognition and highly accurate steering. First order auditory processing occurs in the thorax and pattern recognition in the brain. Local auditory brain neurons are tuned to the structure of the calling song, based on fast integration of inhibitory and excitatory synaptic activity. How pattern recognition is linked to the generation of auditory steering commands still remains an open question.

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References

  • Alexander RD (1962) Evolutionary change in cricket acoustical communication. Evolution 16:443–467

    Article  Google Scholar 

  • Baden T, Hedwig B (2008) Front leg movements and tibial motoneurons underlying auditory steering in the cricket (Gryllus bimaculatus deGeer). J Exp Biol 211: 2123–2133

    Google Scholar 

  • Ball E, Oldfield B, Rudolph K (1989) Auditory organ structure, development, and function. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, London, pp 391–422

    Google Scholar 

  • Bentley D (1977) Control of cricket song patterns by descending interneurons. J Comp Physiol A 116:19–38

    Article  Google Scholar 

  • Bentley DR (1969) Intracellular activity in cricket neurons during the generation of behaviour patterns. J Insect Physiol 15:677–684

    Article  PubMed  CAS  Google Scholar 

  • Danley P, Mullen S, Liu F, Nene V, Quackenbush J, Shaw KL (2007) A cricket gene index: a genomic resource for studying neurobiology, speciation, and molecular evolution. BMC Genomics 8:109. doi:10.1186/1471-2164-8-109

    Article  PubMed  Google Scholar 

  • Doherty JA, Pires A (1987) A new microcomputer-based method for measuring walking phonotaxis in field crickets (Gryllidae). J Exp Biol 130:425–432

    PubMed  CAS  Google Scholar 

  • Edwards CJ, Leary CJ, Rose GJ (2007) Counting on inhibition and rate-dependent excitation in the auditory system. J Neurosci 27:13384–13392

    Article  PubMed  CAS  Google Scholar 

  • Esch H, Huber F, Wohlers DW (1980) Primary auditory neurons in crickets: physiology and central projections. J Comp Physiol A 137:27–38

    Article  Google Scholar 

  • Hedwig B (2000) Control of cricket stridulation by a command neuron: efficacy depends on the behavioral state. J Neurophysiol 83:712–722

    PubMed  CAS  Google Scholar 

  • Hedwig B, Heinrich R (1997) Identified descending brain neurons control different stridulatory motor patterns in an acridid grasshopper. J Comp Physiol A 180:285–294

    Article  Google Scholar 

  • Hedwig B, Poulet J (2005) Mechanisms underlying phonotactic steering in the cricket Gryllus bimaculatus revealed with a fast trackball system. J Exp Biol 208:915–927

    Article  PubMed  CAS  Google Scholar 

  • Hedwig B, Poulet JFA (2004) Complex auditory behaviour emerges from simple reactive steering. Nature 430:781–785

    Article  PubMed  CAS  Google Scholar 

  • Heffner R, Koay G, Heffner H (2007) Sound-localization acuity and its relation to vision in large and small fruit-eating bats: I. Echolocating species, Phyllostomus hastatus and Carollia perspicillata. Hearing Res 234:1–9

    Article  CAS  Google Scholar 

  • Helversen D, Helversen O (1995) Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing? J Comp Physiol A 177:767–774

    Article  Google Scholar 

  • Hennig RM (1990) Neuronal organisation of the flight motor pattern in the cricket, Teleogryllus commodus. J Comp Physiol A 167(5):629–639

    Google Scholar 

  • Hennig R, Otto D (1996) Distributed control of song pattern generation in crickets revealed by lesions to the thoracic ganglia. Zoology 99:268–276

    Google Scholar 

  • Hoy R (1978) Acoustic communication in crickets: a model system for the study of feature detection. Fed Proc 37:2316–2323

    PubMed  CAS  Google Scholar 

  • Huber F (1955) Sitz und Bedeutung nervӧser Zentren für Instinkthandlungen beim Männchen von Gryllus campestris L. Zeitschrift für Tierpsychologie 12:12–48

    Article  Google Scholar 

  • Huber F, Thorson J (1985) Cricket auditory communication. Sci Am 253:46–54

    Article  Google Scholar 

  • Imaizumi K, Pollack GS (2001) Neural representation of sound amplitude by functionally different auditory receptors in crickets. J Acoust Soc Am 109:1247–1260

    Article  PubMed  CAS  Google Scholar 

  • Kostarakos K, Rӧmer H (2010) Sound transmission and directional hearing in field crickets: neurophysiological studies outdoors. J Comp Physiol A 196:1–13

    Google Scholar 

  • Kostarakos K, Hedwig B (2012) Calling song recognition in female crickets: temporal tuning of identified brain neurons matches behaviour. J Neurophysiol 32:9601–9612

    CAS  Google Scholar 

  • Kupfermann I, Weiss KR (1978) The command neuron concept. Behav Brain Sci 1:3–10

    Article  Google Scholar 

  • Kutsch W (1969) Neuromuskuläre Aktivität bei verschiedenen Verhaltensweisen von drei Grillenarten. J Comp Physiol A 63:335–378

    Google Scholar 

  • Kutsch W, Huber F (1989) Neural basis of song production. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, London, pp 262–309

    Google Scholar 

  • Larsen O, Kleindienst B, Michelsen A (1989) Biophysical aspects of sound perception. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, London, pp 364–390

    Google Scholar 

  • Mason AC, Oshinsky ML, Hoy RR (2001) Hyperacute directional hearing in a microscale auditory system. Nature 410:686–690

    Article  PubMed  CAS  Google Scholar 

  • Michelsen A (1992) Hearing and sound communication in small animals: evolutionary adaptations to the laws of physics. In: Webster DB, Fay RR, An Popper (eds) The evolutionary biology of hearing. Springer, Berlin, pp 61–77

    Chapter  Google Scholar 

  • Michelsen A, Löhe G (1995) Tuned directionality in cricket ears. Nature 375:639

    Article  CAS  Google Scholar 

  • Michelsen A, Popov A, Lewis B (1994) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175:153–164

    Article  Google Scholar 

  • Montealegre-Z F, Jonsson T, Robert D (2011) Sound radiation and wing mechanics in stridulating field crickets (Orthoptera: Gryllidae). J Exp Biol 214:2105–2117

    Article  PubMed  Google Scholar 

  • Murphey R, Zaretsky M (1972) Orientation to calling song by female crickets, Scapsipedus marginatus (Gryllidae). J Exp Biol 56:335–352

    PubMed  CAS  Google Scholar 

  • Nakamura T, Yoshizaki M, Ogawa S, Okamoto H, Shinmyo Y, Bando T, Ohuchi H, Noji S, Mito T (2010) Imaging of transgenic cricket embryos reveals cell movements consistent with a syncytial patterning mechanism. Curr Biol 20:1641–1647

    Article  PubMed  CAS  Google Scholar 

  • Nocke H (1972) Physiological aspects of sound communication in crickets (Gryllus campestris L.). J Comp Physiol A 80:141–162

    Article  Google Scholar 

  • Nolen T, Hoy R (1984) Initiation of behavior by single neurons: the role of behavioral context. Science 226:992

    Article  PubMed  CAS  Google Scholar 

  • Olshausen BA, Field DJ (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 14:481–487

    Article  PubMed  CAS  Google Scholar 

  • Otte D (1992) Evolution of cricket songs. J Orthop Res 1:25–49

    Google Scholar 

  • Otto D (1971) Untersuchungen zur zentralnervӧsen kontrolle der lauterzeugung von grillen. J Comp Physiol A 74:227–271

    Google Scholar 

  • Otto D (1978) Änderungen von Gesangsparametern bei der Grille (Gryllus campestris L.) nach Injektion von Pharmaka ins Gehirn. Verh Dtsch Zool Ges 245

    Google Scholar 

  • Otto D, Hennig R (1993) Interneurons descending from the cricket subesophageal ganglion control stridulation and ventilation. Naturwissenschaften 80:36–38

    Article  Google Scholar 

  • Perkel DH, Mulloney B (1974) Motor pattern production in reciprocally inhibitory neurons exhibiting postinhibitory rebound. Science 185:181–183

    Article  PubMed  CAS  Google Scholar 

  • Petrou G, Webb B (2012) Detailed tracking of body and leg movements of a freely walking female cricket during phonotaxis. J Neurosci Meth 203:56–68

    Article  Google Scholar 

  • Pollack G (2000) Who, what, where? recognition and localization of acoustic signals by insects. Curr Opin Neurobiol 10:763–767

    Article  PubMed  CAS  Google Scholar 

  • Pollack G, Faulkes Z (1998) Representation of behaviorally relevant sound frequencies by auditory receptors in the cricket Teleogryllus oceanicus. J Exp Biol 201:155–163

    PubMed  Google Scholar 

  • Pollack GS (1988) Selective attention in an insect auditory neuron. J Neurosci 8:2635–2639

    PubMed  CAS  Google Scholar 

  • Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429

    Article  PubMed  CAS  Google Scholar 

  • Popov A, Shuvalov V, Svetlogorskaya I, Markovich A (1974) Acoustic behaviour and auditory system in insects. In: J. Schwartzkopff, (ed) Mechanoreception. Abh Rheinisch-Westfäl Akad Wiss, vol 53. pp 281–306

    Google Scholar 

  • Poulet JFA, Hedwig B (2002) A corollary discharge maintains auditory sensitivity during sound production. Nature 418:872–876

    Article  PubMed  CAS  Google Scholar 

  • Poulet JFA, Hedwig B (2006) The cellular basis of a corollary discharge. Science 311:518

    Article  PubMed  CAS  Google Scholar 

  • Poulet JFA, Hedwig B (2005) Auditory orientation in crickets: pattern recognition controls reactive steering. Proc Nat Acad Sci 102:15665–15669

    Article  PubMed  CAS  Google Scholar 

  • Reeve RE, Webb BH (2003) New neural circuits for robot phonotaxis. Phil Trans Roy Soc London A 361:2245–2266

    Article  Google Scholar 

  • Regen J (1913) Ueber die anlockung des weibchens von Gryllus campestris L. durch telephonisch übertragene Stridulationslaute des Männchens. Pflüg Archiv Europ J Physiol 155:193–200

    Article  Google Scholar 

  • Rheinlaender J, Blätgen G (1982) The precision of auditory lateralization in the cricket, Gryllus bimaculatus. Physiol Entomol 7:209–218

    Article  Google Scholar 

  • Roesel von Rosenhof AJ (1749) Insectenbelustigung zweyter Theil, welcher acht Klassen verschiedener sowohl inlaendischer als auch einiger auslaendischer Insecten enthaelt. Nuernberg, Fleischmann JJ

    Google Scholar 

  • Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog. Science 219:1087–1089

    Article  PubMed  CAS  Google Scholar 

  • Rose GJ, Leary CJ, Edwards CJ (2011) Interval-counting neurons in the anuran auditory midbrain: factors underlying diversity of interval tuning. J Comp Physiol A 197:97–108

    Article  Google Scholar 

  • Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185

    Article  Google Scholar 

  • Schildberger K, Hӧrner M (1988) The function of auditory neurons in cricket phonotaxis I. Influence of hyperpolarization of identified neurons on sound localization. J Comp Physiol A 163:621–631

    Article  Google Scholar 

  • Schildberger K, Huber F, Wohlers D (1989) Central auditory pathway: neuronal correlates of phonotactic behavior. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, London, pp 423–458

    Google Scholar 

  • Schmitz B, Scharstein H, Wendler G (1982) Phonotaxis in Gryllus campestris L. (Orthoptera, Gryllidae). J Comp Physiol A 148:431–444

    Article  Google Scholar 

  • Schöneich S, Hedwig B (2010) Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer). PLoS ONE 5(12):e15141

    Article  PubMed  Google Scholar 

  • Schöneich S, Hedwig B (2011) Neural basis of singing in crickets: central pattern generation in abdominal ganglia. Naturwissenschaften 98(12):1069–1073

    Article  PubMed  Google Scholar 

  • Schöneich S, Hedwig B (2012) Cellular basis for singing motor pattern generation in the field cricket (Gryllus bimaculatus DeGeer). Brain Behav 2(6):707–725

    Article  PubMed  Google Scholar 

  • Sobel EC, Tank DW (1994) In vivo Ca2+ dynamics in a cricket auditory neuron: an example of chemical computation. Science 263:823–826

    Article  PubMed  CAS  Google Scholar 

  • Staudacher E (1998) Distribution and morphology of descending brain neurons in the cricket Gryllus bimaculatus. Cell Tiss Res 294:187–202

    Article  Google Scholar 

  • Staudacher E, Schildberger K (1998) Gating of sensory responses of descending brain neurones during walking in crickets. J Exp Biol 201:559–572

    Google Scholar 

  • Staudacher EM (2001) Sensory responses of descending brain neurons in the walking cricket, Gryllus bimaculatus. J Comp Physiol A 187:1–17

    Article  PubMed  CAS  Google Scholar 

  • Stumpner A, von Helversen D (2001) Evolution and function of auditory systems in insects. Naturwissenschaften 88:159–170

    Article  PubMed  CAS  Google Scholar 

  • Stout JF, DeHaan CH, McGhee RW (1983) Attractiveness of the male Acheta domesticus calling song to females I. Dependence on each of the calling song features. J Comp Physiol A 153:509–521

    Article  Google Scholar 

  • Thorson J, Weber T, Huber F (1982) Auditory behavior of the cricket II. Simplicity of calling-song recognition in Gryllus and anomalous phonotaxis at abnormal frequencies. J Comp Physiol A 146:361–378

    Article  Google Scholar 

  • Tschuch G (1977) Der Einfluss synthetischer Gesänge auf die Weibchen von Gryllus bimaculatus de Geer (Teil 2). Zool Jb Physiol 81:360–372

    Google Scholar 

  • Ulagaraj S, Walker TJ (1973) Phonotaxis of crickets in flight: attraction of male and female crickets to male calling songs. Science 182:1278–1279

    Article  PubMed  CAS  Google Scholar 

  • Weber T, Thorson J (1989) Phonotactic behavior of walking crickets. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, London, pp 310–339

    Google Scholar 

  • Wendler G, Dambach M, Schmitz B, Scharstein H (1980) Analysis of the acoustic orientation behavior in crickets (Gryllus campestris L.). Naturwissenschaften 67:99–101

    Article  Google Scholar 

  • Wenzel B, Hedwig B (1999) Neurochemical control of cricket stridulation revealed by pharmacological microinjections into the brain. J Exp Biol 202:2203–2216

    PubMed  CAS  Google Scholar 

  • Wiese K, Eilts-Grimm K (1985) Functional potential of recurrent lateral inhibition in cricket audition. In: Kalmring K, Elsner N (eds) Acoustic and vibrational communication in insects. Parey, Berlin, pp 33–40

    Google Scholar 

  • Witney AG, Hedwig B (2011) Kinematics of phonotactic steering in the walking cricket Gryllus bimaculatus (de Geer). J Exp Biol 214:69–79

    Article  PubMed  Google Scholar 

  • Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket, Gryllus campestris L. J Comp Physiol A 146:161–173

    Article  Google Scholar 

  • Wyttenbach RA, May ML, Hoy RR (1996) Categorical perception of sound frequency by crickets. Science 273:1542–1544

    Article  PubMed  CAS  Google Scholar 

  • Zorovic M, Hedwig B (2011) Processing of species-specific auditory patterns in the cricket brain by ascending, local, and descending neurons during standing and walking. J Neurophysiol 105:2181–2194

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

I am grateful to the members of the lab that contributed to the presented data and fruitful discussions: Stefan Schöneich, Kostas Kostarakos, Hannah ter Hofstede, James Poulet, Tom Baden and Alice Witney and also to the BBSRC, the Isaac Newton Trust and the Royal Society for funding.

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  1. Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK

    Berthold Hedwig

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    Berthold Hedwig

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Hedwig, B. (2014). Towards an Understanding of the Neural Basis of Acoustic Communication in Crickets. In: Hedwig, B. (eds) Insect Hearing and Acoustic Communication. Animal Signals and Communication, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-40462-7_8

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