Computational principles underlying recognition of acoustic signals in grasshoppers and crickets

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.

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References

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

    Article  Google Scholar 

  2. Atick JJ, Redlich AN (1990) Towards a theory of early visual processing. Neural Comput 2:308–320

    Article  Google 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 187:255–264

    CAS  PubMed  Article  Google 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 165:687–695

    Google Scholar 

  5. Bell AJ, Sejnowski TJ (1997) The ‘independent components’ of natural scenes are edge filters. Vis Res 37:3327–3338

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  6. Boyan GS (1992) Common synaptic drive to segmentally homologous interneurons in the locust. J Comp Neurol 321:544–554

    CAS  PubMed  Article  Google Scholar 

  7. Boyan GS (1999) presynaptic contributions to response shape in an auditory neuron of the grasshopper. J Comp Physiol A 184:279–294

    Article  Google Scholar 

  8. Bush SL, Schul J (2006) Pulse-rate recognition in an insect: evidence of a role for oscillatory neurons. J Comp Physiol A 192:113–121

    Article  Google 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 212:648–655

    PubMed  Article  Google Scholar 

  10. Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comput Neurosci 35:75–85

    PubMed  Article  Google Scholar 

  11. Clemens J, Ronacher B (2013) Feature extraction and integration underlying perceptual decision making during courtship in grasshoppers. J Neurosci 33:12136–12145

    CAS  PubMed  Article  Google 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 108:13812–13817

    CAS  PubMed Central  PubMed  Article  Google 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 32:10053–10062

    CAS  PubMed  Article  Google 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 22:1493–1510

    PubMed  Article  Google 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: 2:1160–1169

    CAS  Article  Google Scholar 

  16. Deily JA, Schul J (2009) Selective phonotaxis in Neoconocephalus nebrascensis (Orthoptera: Tettigoniidae): call recognition at two temporal scales. J Comp Physiol A 195:31–37

    Article  Google 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 92:1–17

    Article  Google 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):791–799

    Article  Google Scholar 

  19. Elsner N, Popov AV (1978) Neuroethology of acoustic communication. Adv Insect Physiol 13:229–355

    Article  Google 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 82:384–386

    CAS  Google Scholar 

  21. Flook PK, Rowell CHF (1997) The phylogeny of the Caelifera (Insecta, Orthoptera) as deduced from mtrRNA gene sequences. Mol Genet Evol 8:89–103

    CAS  Google Scholar 

  22. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, Chicago

    Google Scholar 

  23. Gottsberger B, Mayer F (2007) Behavioral sterility of hybrid males in acoustically communicating grasshoppers. J Comp Physiol A 193:703–714

    Article  Google 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 215:1681–1690

    Article  Google Scholar 

  25. Hedwig B (1994) A cephalothoracic command system controls stridulation in the acridid grasshopper Omocestus viridulus L. J Neurophysiol 72:2015–2025

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google 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 137–152

    Google Scholar 

  28. Hennig RM (2003) Acoustic feature extraction by cross-correlation in crickets? J Comp Physiol A 189:589–598

    CAS  Article  Google 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 195:971–987

    Article  Google 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 180:621–630

    Article  Google Scholar 

  31. Hennig RM, Franz A, Stumpner A (2004) Processing of auditory information in insects. Microsc Res Tech 63:351–374

    CAS  PubMed  Article  Google 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 12:355–375

    CAS  PubMed  Article  Google Scholar 

  34. Hoy RR, Popper AN, Fay RR (eds) (1998) Comparative hearing: insects. Springer, New York

    Google Scholar 

  35. Imaizumi K, Pollack GS (2005) Central projections of auditory receptor neurons of crickets. J Comp Neurol 493:439–447

    PubMed  Article  Google 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 283:270–285

    Article  Google 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):9601–9612

    CAS  PubMed  Article  Google Scholar 

  38. Marsat G, Pollack GS (2006) A behavioural role for feature detection by sensory bursts. J Neurosci 26:10542–10547

    CAS  PubMed  Article  Google Scholar 

  39. Meyer J, Elsner N (1996) How well are frequency sensitivities of grasshopper ears tuned to species-specific song spectra? J Exp Biol 199:1631–1642

    PubMed  Google 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 18–62

    Google Scholar 

  41. 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 

  42. Mitchell M (1998) An introduction to genetic algorithms (complex adaptive systems), 3rd edn. MIT, Cambridge

    Google 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 197:251–265

    Article  Google Scholar 

  44. Olshausen BA, Field DJ (1996) Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature 381:607–609

    CAS  PubMed  Article  Google Scholar 

  45. Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429–432

    CAS  PubMed  Article  Google Scholar 

  46. Priebe NJ, Ferster D (2012) Mechanisms of neuronal computation in mammalian visual cortex. Neuron 75:194–208

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  47. Römer H (1976) Die Informationsverarbeitung tympanaler Rezeptorelemente von Locusta migratoria. J Comp Physiol A 109:101–122

    Article  Google Scholar 

  48. Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Physiol A 155:249–262

    Article  Google 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 185–204

    Google 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 189:419–425

    CAS  Article  Google 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 183:729–735

    Article  Google 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 163:517–523

    Article  Google 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 158:363–374

    Article  Google 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 186:1065–1072

    CAS  PubMed  Article  Google 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):e43975

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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

    Article  Google 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 163:621–631

    Article  Google 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 194:221–233

    CAS  Article  Google 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):707–725

    PubMed Central  PubMed  Article  Google 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 180:573–583

    Article  Google Scholar 

  61. Schul J (1998) Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia). J Comp Physiol A 183:401–410

    Article  Google 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 167–184

    Google 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 5:427–435

    Article  Google Scholar 

  64. Smith EC, Lewicki MS (2006) Efficient auditory coding. Nature 439:978–982

    CAS  PubMed  Article  Google 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 5–26

    Google 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-Nürnberg

  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 143–166

    Google 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 158:391–410

    Google Scholar 

  69. Stumpner A, Ronacher B (1994) Neurophysiological aspects of song pattern recognition and sound localization in grasshoppers. Am Zool 34:696–705

    Google 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 171:405–412

    Article  Google 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 6:1–23

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google 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 158:411–430

    Google Scholar 

  74. Triblehorn JD, Schul J (2009) Sensory-encoding differences contribute to species-specific call recognition mechanisms. J Neurophysiol 102:1348–1357

    CAS  PubMed Central  PubMed  Article  Google 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 24:1039–1049

    CAS  PubMed  Article  Google 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 93:3548–3559

    CAS  PubMed  Article  Google Scholar 

  77. von Helversen D (1972) Gesang des Männchens und Lautschema des Weibchens bei der Feldheuschrecke Chorthippus biguttulus (Orthoptera, Acrididae). J Comp Physiol 81:381–422

    Article  Google Scholar 

  78. von Helversen O (1986) Gesang und Balz bei Feldheuschrecken der Chorthippus albomarginatus-Gruppe. Zool Jahrb Systematik 113:319–342

    Google Scholar 

  79. von Helversen D (1997) Acoustic communication and orientation in grasshoppers. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser, Basel, pp 301–341

    Google 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 253–284

    Google 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 180:373–386

    Article  Google Scholar 

  82. von Helversen D, von Helversen O (1998) Acoustic pattern recognition in a grasshopper: processing in the frequency or time domain? Biol Cybern 79:467–476

    Article  Google 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 146:161–173

    Article  Google Scholar 

  84. Wohlgemuth S, Ronacher B (2007) Auditory discrimination of amplitude modulations based on metric distances of spike trains. J Neurophysiol 97:3082–3092

    PubMed  Article  Google 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 197:61–74

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google 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:e1002123

    CAS  PubMed Central  PubMed  Article  Google 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 105:2181–2194

    PubMed Central  PubMed  Article  Google Scholar 

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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).

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Ronacher, B., Hennig, R.M. & Clemens, J. Computational principles underlying recognition of acoustic signals in grasshoppers and crickets. J Comp Physiol A 201, 61–71 (2015). https://doi.org/10.1007/s00359-014-0946-7

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Keywords

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