Journal of Comparative Physiology A

, Volume 201, Issue 1, pp 61–71 | Cite as

Computational principles underlying recognition of acoustic signals in grasshoppers and crickets

  • Bernhard Ronacher
  • R. Matthias Hennig
  • Jan Clemens
Review

Abstract

Grasshoppers and crickets independently evolved hearing organs and acoustic communication. They differ considerably in the organization of their auditory pathways, and the complexity of their songs, which are essential for mate attraction. Recent approaches aimed at describing the behavioral preference functions of females in both taxa by a simple modeling framework. The basic structure of the model consists of three processing steps: (1) feature extraction with a bank of ‘LN models’—each containing a linear filter followed by a nonlinearity, (2) temporal integration, and (3) linear combination. The specific properties of the filters and nonlinearities were determined using a genetic learning algorithm trained on a large set of different song features and the corresponding behavioral response scores. The model showed an excellent prediction of the behavioral responses to the tested songs. Most remarkably, in both taxa the genetic algorithm found Gabor-like functions as the optimal filter shapes. By slight modifications of Gabor filters several types of preference functions could be modeled, which are observed in different cricket species. Furthermore, this model was able to explain several so far enigmatic results in grasshoppers. The computational approach offered a remarkably simple framework that can account for phenotypically rather different preference functions across several taxa.

Keywords

Perceptual decision making Linear–nonlinear model Gabor filter Behavioral preference functions Acoustic communication 

Notes

Acknowledgments

We thank many members of the Behavioral Physiology lab for sharing their behavioral data, in particular Stefanie Krämer, Olaf Kutzki, and Jana Sträter. This work was funded by grants to BR from the Federal Ministry of Education and Research, Germany (01GQ0410, 01GQ1001A), the Deutsche Forschungsgemeinschaft (SFB618 grants to BR and RMH; Ro 547/12-1; GK1589/1 grant to JC) and the German Academic Exchange Service (JC).

References

  1. Alexander RD (1962) Evolutionary change in cricket acoustical communication. Evolution 16:443–467CrossRefGoogle Scholar
  2. Atick JJ, Redlich AN (1990) Towards a theory of early visual processing. Neural Comput 2:308–320CrossRefGoogle Scholar
  3. Balakrishnan R, von Helversen D, von Helversen O (2001) Song pattern recognition in the grasshopper Chorthippus biguttulus: the mechanisms of syllable onset and offset detection. J Comp Physiol A 187:255–264PubMedCrossRefGoogle Scholar
  4. Bauer M, von Helversen O (1987) Separate localisation of sound recognizing and sound producing neural mechanisms in a grasshopper. J Comp Physiol A 165:687–695Google Scholar
  5. Bell AJ, Sejnowski TJ (1997) The ‘independent components’ of natural scenes are edge filters. Vis Res 37:3327–3338PubMedCentralPubMedCrossRefGoogle Scholar
  6. Boyan GS (1992) Common synaptic drive to segmentally homologous interneurons in the locust. J Comp Neurol 321:544–554PubMedCrossRefGoogle Scholar
  7. Boyan GS (1999) presynaptic contributions to response shape in an auditory neuron of the grasshopper. J Comp Physiol A 184:279–294CrossRefGoogle Scholar
  8. Bush SL, Schul J (2006) Pulse-rate recognition in an insect: evidence of a role for oscillatory neurons. J Comp Physiol A 192:113–121CrossRefGoogle Scholar
  9. Bush SL, Beckers OM, Schul J (2009) A complex mechanism of call recognition in the katydid Neoconocephalus affinis (Orthoptera: Tettigoniidae). J Exp Biol 212:648–655PubMedCrossRefGoogle Scholar
  10. Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comput Neurosci 35:75–85PubMedCrossRefGoogle Scholar
  11. Clemens J, Ronacher B (2013) Feature extraction and integration underlying perceptual decision making during courtship in grasshoppers. J Neurosci 33:12136–12145PubMedCrossRefGoogle Scholar
  12. Clemens J, Kutzki O, Ronacher B, Schreiber S, Wohlgemuth S (2011) Efficient transformation of an auditory population code in a small sensory system. Proc Natl Acad Sci USA 108:13812–13817PubMedCentralPubMedCrossRefGoogle Scholar
  13. Clemens J, Wohlgemuth S, Ronacher B (2012) Nonlinear computations underlying temporal and population sparseness in the auditory system of the grasshopper. J Neurosci 32:10053–10062PubMedCrossRefGoogle Scholar
  14. Creutzig F, Benda J, Wohlgemuth S, Stumpner A, Ronacher B, Herz AVM (2010) Timescale-invariant pattern recognition by feed-forward inhibition and parallel signal processing. Neural Comput 22:1493–1510PubMedCrossRefGoogle Scholar
  15. Daugman JG (1985) Uncertainty relation for resolution in space, spatial frequency and orientation optimized by two-dimensional visual cortical filters. J Opt Soc Am A: 2:1160–1169CrossRefGoogle Scholar
  16. Deily JA, Schul J (2009) Selective phonotaxis in Neoconocephalus nebrascensis (Orthoptera: Tettigoniidae): call recognition at two temporal scales. J Comp Physiol A 195:31–37CrossRefGoogle Scholar
  17. Eibl E, Huber F (1979) Central projections of tibial sensory fibers within the three thoracic ganglia of crickets (G. campestris L., G. bimaculatus DeGeer). Zoomorphology 92:1–17CrossRefGoogle Scholar
  18. Einhäupl A, Stange N, Hennig RM, Ronacher B (2011) Attractiveness of grasshopper songs correlates with their robustness against noise. Behav Ecol 22(4):791–799CrossRefGoogle Scholar
  19. Elsner N, Popov AV (1978) Neuroethology of acoustic communication. Adv Insect Physiol 13:229–355CrossRefGoogle Scholar
  20. Elsner N, Wasser G (1995) The transition from leg to wing stridulation in two geographically distinct populations of the grasshopper Stenobothrus rubicundus. Naturwissenschaften 82:384–386Google Scholar
  21. Flook PK, Rowell CHF (1997) The phylogeny of the Caelifera (Insecta, Orthoptera) as deduced from mtrRNA gene sequences. Mol Genet Evol 8:89–103Google Scholar
  22. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, ChicagoGoogle Scholar
  23. Gottsberger B, Mayer F (2007) Behavioral sterility of hybrid males in acoustically communicating grasshoppers. J Comp Physiol A 193:703–714CrossRefGoogle Scholar
  24. Grobe B, Rothbart MM, Hanschke A, Hennig RM (2012) Auditory processing at two time scales by the cricket Gryllus bimaculatus. J Expl Biol 215:1681–1690CrossRefGoogle Scholar
  25. Hedwig B (1994) A cephalothoracic command system controls stridulation in the acridid grasshopper Omocestus viridulus L. J Neurophysiol 72:2015–2025PubMedGoogle Scholar
  26. Hedwig B (2000) Control of cricket stridulation by a command neuron: efficacy depends on behavioural state. J Neurophysiol 83:712–722PubMedGoogle Scholar
  27. Heller K-G (2006) Song evolution and speciation in bushcrickets. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution. CRC Press, Boca Raton, pp 137–152Google Scholar
  28. Hennig RM (2003) Acoustic feature extraction by cross-correlation in crickets? J Comp Physiol A 189:589–598CrossRefGoogle Scholar
  29. Hennig RM (2009) Walking in Fourier’s space: algorithms for the computation of periodicities in song patterns by the cricket Gryllus bimaculatus. J Comp Physiol A 195:971–987CrossRefGoogle Scholar
  30. Hennig RM, Weber T (1997) Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis. J Comp Physiol A 180:621–630CrossRefGoogle Scholar
  31. Hennig RM, Franz A, Stumpner A (2004) Processing of auditory information in insects. Microsc Res Tech 63:351–374PubMedCrossRefGoogle Scholar
  32. Hennig RM, Heller K-G, Clemens J (2014) Time and timing in the acoustic recognition system of crickets Front Physiol 5:286. doi: 10.3389/fphys.2014.00286
  33. Hoy RR (1989) Startle, categorical response, and attention in acoustic behavior of insects. Ann Rev Neurosci 12:355–375PubMedCrossRefGoogle Scholar
  34. Hoy RR, Popper AN, Fay RR (eds) (1998) Comparative hearing: insects. Springer, New YorkGoogle Scholar
  35. Imaizumi K, Pollack GS (2005) Central projections of auditory receptor neurons of crickets. J Comp Neurol 493:439–447PubMedCrossRefGoogle Scholar
  36. Jacobs K, Otte B, Lakes-Harlan R (1999) Tympanal receptor cells of Schistocerca gregaria: correlation of soma positions and dendrite attachment sites, central projections and physiologies. J Exp Zool 283:270–285CrossRefGoogle Scholar
  37. Kostarakos K, Hedwig B (2012) Calling song recognition in female crickets: temporal tuning of identified brain neurons matches behavior. J Neurosci 32(28):9601–9612PubMedCrossRefGoogle Scholar
  38. Marsat G, Pollack GS (2006) A behavioural role for feature detection by sensory bursts. J Neurosci 26:10542–10547PubMedCrossRefGoogle Scholar
  39. Meyer J, Elsner N (1996) How well are frequency sensitivities of grasshopper ears tuned to species-specific song spectra? J Exp Biol 199:1631–1642PubMedGoogle Scholar
  40. Michelsen A (1998) Biophysics of sound localization in insects. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, Berlin, pp 18–62CrossRefGoogle Scholar
  41. Michelsen A, Popov A, Lewis B (1994) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175:153–164CrossRefGoogle Scholar
  42. Mitchell M (1998) An introduction to genetic algorithms (complex adaptive systems), 3rd edn. MIT, CambridgeGoogle Scholar
  43. Neuhofer D, Stemmler M, Ronacher B (2011) Neuronal precision and the limits for acoustic signal recognition in a small neuronal network. J Comp Physiol A 197:251–265CrossRefGoogle Scholar
  44. Olshausen BA, Field DJ (1996) Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature 381:607–609PubMedCrossRefGoogle Scholar
  45. Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429–432PubMedCrossRefGoogle Scholar
  46. Priebe NJ, Ferster D (2012) Mechanisms of neuronal computation in mammalian visual cortex. Neuron 75:194–208PubMedCentralPubMedCrossRefGoogle Scholar
  47. Römer H (1976) Die Informationsverarbeitung tympanaler Rezeptorelemente von Locusta migratoria. J Comp Physiol A 109:101–122CrossRefGoogle Scholar
  48. Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Physiol A 155:249–262CrossRefGoogle Scholar
  49. Ronacher B (2014) Processing of species-specific signals in the auditory pathway of grasshoppers. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication, vol 1. Springer, Berlin, pp 185–204CrossRefGoogle Scholar
  50. Ronacher B, Hoffmann C (2003) Influence of amplitude modulated noise on the recognition of communication signals in the grasshopper Chorthippus biguttulus. J Comp Physiol A 189:419–425CrossRefGoogle Scholar
  51. Ronacher B, Krahe R (1998) Song recognition in the grasshopper Chorthippus biguttulus is not impaired by shortening song signals: implications for neuronal encoding. J Comp Physiol A 183:729–735CrossRefGoogle Scholar
  52. Ronacher B, Stumpner A (1988) Filtering of behaviourally relevant temporal parameters of a grasshopper’s song by an auditory interneuron. J Comp Physiol A 163:517–523CrossRefGoogle Scholar
  53. Ronacher B, von Helversen D, von Helversen O (1986) Routes and stations in the processing of auditory directional information in the CNS of a grasshopper, as revealed by surgical experiments. J Comp Physiol A 158:363–374CrossRefGoogle Scholar
  54. Ronacher B, Krahe R, Hennig RM (2000) Effects of signal duration on the recognition of masked communication signals by the grasshopper Chorthippus biguttulus. J Comp Physiol A 186:1065–1072PubMedCrossRefGoogle Scholar
  55. Rothbart MM, Hennig RM (2012) The Steppengrille (Gryllus spec./assimilis): selective filters and signal mismatch on two time scales. PLoS One 7(9):e43975PubMedCentralPubMedCrossRefGoogle Scholar
  56. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185CrossRefGoogle Scholar
  57. Schildberger K, Hörner M (1988) The function of auditory neurons in cricket phonotaxis. I. Influence of hyperpolarization of identified neurons on sound localization. J Comp Physiol A 163:621–631CrossRefGoogle Scholar
  58. Schmidt A, Ronacher B, Hennig RM (2008) The role of frequency, phase and time for processing amplitude modulated signals by grasshoppers. J Comp Physiol A 194:221–233CrossRefGoogle Scholar
  59. Schöneich S, Hedwig B (2012) Cellular basis for singing motor pattern generation in the field cricket (Gryllus bimaculatus DeGeer). Brain Behav 2(6):707–725PubMedCentralPubMedCrossRefGoogle Scholar
  60. Schul J (1997) Neuronal basis of phonotactic behaviour in Tettigonia viridissima: processing of behaviourally relevant signals by auditory afferents and thoracic interneurons. J Comp Physiol A 180:573–583CrossRefGoogle Scholar
  61. Schul J (1998) Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia). J Comp Physiol A 183:401–410CrossRefGoogle Scholar
  62. Schul J, Bush S, Frederick KH (2014) Evolution of call patterns and pattern recognition mechanisms in Neoconocephalus katydids. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication, vol 1. Springer, Berlin, pp 167–184CrossRefGoogle Scholar
  63. Silver S, Kalmring K, Kühne R (1980) The responses of central acoustic and vibratory interneurones in bushcrickets and locusts to ultrasonic stimulation. Physiol Entomol 5:427–435CrossRefGoogle Scholar
  64. Smith EC, Lewicki MS (2006) Efficient auditory coding. Nature 439:978–982PubMedCrossRefGoogle Scholar
  65. Strauß J, Lakes-Harlan R (2014) Evolutionary and phylogenetic origins of tympanal hearing organs in insects. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication. vol 1. Springer, Berlin, pp 5–26CrossRefGoogle Scholar
  66. Stumpner A (1988) Auditorische thorakale Interneurone von Chorthippus biguttulus L.: Morphologische und physiologische Charakterisierung und Darstellung ihrer Filtereigenschaften für verhaltensrelevante Lautattrappen. PhD thesis, Universität Erlangen-NürnbergGoogle Scholar
  67. Stumpner A, Nowotny M (2014) Neural processing in the bush-cricket auditory pathway. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication, vol 1. Springer, Berlin, pp 143–166CrossRefGoogle Scholar
  68. Stumpner A, Ronacher B (1991) Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus: I. Morphological and physiological characterization. J Exp Biol 158:391–410Google Scholar
  69. Stumpner A, Ronacher B (1994) Neurophysiological aspects of song pattern recognition and sound localization in grasshoppers. Am Zool 34:696–705Google Scholar
  70. Stumpner A, von Helversen O (1992) Recognition of a two-element song in a grasshopper Chorthippus dorsatus (Orthoptera: Gomphocerinae). J Comp Physiol A 171:405–412CrossRefGoogle Scholar
  71. Stumpner A, von Helversen O (1994) Song production and song recognition in a group of sibling grasshopper species (Chorthippus dorsatus, C. dichrous, and C. loratus: Orthoptera, Acrididae). Bioacoustics 6:1–23CrossRefGoogle Scholar
  72. Stumpner A, von Helversen D (2001) Evolution and function of auditory systems in insects. Naturwissenschaften 88:159–170PubMedCrossRefGoogle Scholar
  73. Stumpner A, Ronacher B, von Helversen O (1991) Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus 2. Processing of temporal patterns of the song of the male. J Exp Biol 158:411–430Google Scholar
  74. Triblehorn JD, Schul J (2009) Sensory-encoding differences contribute to species-specific call recognition mechanisms. J Neurophysiol 102:1348–1357PubMedCentralPubMedCrossRefGoogle Scholar
  75. Vaughan AG, Zhou C, Manoli DS, Baker BS (2014) Neural pathways for the detection and discrimination of conspecific song in D. melanogaster. Curr Biol 24:1039–1049PubMedCrossRefGoogle Scholar
  76. Vogel A, Hennig RM, Ronacher B (2005) Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J Neurophysiol 93:3548–3559PubMedCrossRefGoogle Scholar
  77. von Helversen D (1972) Gesang des Männchens und Lautschema des Weibchens bei der Feldheuschrecke Chorthippus biguttulus (Orthoptera, Acrididae). J Comp Physiol 81:381–422CrossRefGoogle Scholar
  78. von Helversen O (1986) Gesang und Balz bei Feldheuschrecken der Chorthippus albomarginatus-Gruppe. Zool Jahrb Systematik 113:319–342Google Scholar
  79. von Helversen D (1997) Acoustic communication and orientation in grasshoppers. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser, Basel, pp 301–341CrossRefGoogle Scholar
  80. von Helversen O, von Helversen D (1994) Forces driving coevolution of song and song recognition in grasshoppers. In: Schildberger K, Elsner N (eds) Neural basis of behavioural adaptations. G. Fischer, Stuttgart, pp 253–284Google Scholar
  81. von Helversen D, von Helversen O (1997) Recognition of sex in the acoustic communication of the grasshopper Chorthippus biguttulus (Orthoptera, Acrididae). J Comp Physiol A 180:373–386CrossRefGoogle Scholar
  82. von Helversen D, von Helversen O (1998) Acoustic pattern recognition in a grasshopper: processing in the frequency or time domain? Biol Cybern 79:467–476CrossRefGoogle Scholar
  83. Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the crickets Gryllus campestris L. J Comp Physiol 146:161–173CrossRefGoogle Scholar
  84. Wohlgemuth S, Ronacher B (2007) Auditory discrimination of amplitude modulations based on metric distances of spike trains. J Neurophysiol 97:3082–3092PubMedCrossRefGoogle Scholar
  85. Wohlgemuth S, Vogel A, Ronacher B (2011) Encoding of amplitude modulations by auditory neurons of the locust: influence of modulation frequency, rise time, and modulation depth. J Comp Physiol A 197:61–74CrossRefGoogle Scholar
  86. Wyttenbach RA, May ML, Hoy RR (1996) Categorical perception of sound frequency by crickets. Science 273:1542–1544PubMedCrossRefGoogle Scholar
  87. Zhao L, Zhaoping L (2011) Understanding auditory spectro-temporal receptive fields and their changes with input statistics by efficient coding principles. PLoS Comput Biol 7:e1002123PubMedCentralPubMedCrossRefGoogle Scholar
  88. Zorović 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 105:2181–2194PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Bernhard Ronacher
    • 1
  • R. Matthias Hennig
    • 1
  • Jan Clemens
    • 1
    • 2
  1. 1.Department of Biology, Behavioral Physiology GroupHumboldt-Universität zu BerlinBerlinGermany
  2. 2.Princeton Neuroscience InstitutePrinceton UniversityPrincetonUSA

Personalised recommendations