Encyclopedia of Computational Neuroscience

Living Edition
| Editors: Dieter Jaeger, Ranu Jung

Auditory Processing in Insects

Living reference work entry
DOI: https://doi.org/10.1007/978-1-4614-7320-6_321-1

Synonyms

Definition

Auditory processing in insects serves to extract relevant information from acoustic signals about identity and location of acoustic objects, usually in the context of mate attraction and predator avoidance. For this goal, insects process spectral information from the carrier frequency of a signal and obtain temporal information from the sound’s amplitude modulation pattern (the envelope). Auditory processing in insects is constrained by size in several aspects: first, the signal often contains ultrasonic frequencies due to small sender size; second, for localization, insects have only poor directional cues because of the small distance between their ears; and third, due to their small brains, the auditory processing capacity is limited to a small number of neurons.

Detailed Description

Overview and Background

Large Diversity of Hearing Insects and Their Ears

The sense of hearing has evolved in vertebrates and arthropods, and hearing organs...

Keywords

Fractionation Expense Autocorrelation Sine 
This is a preview of subscription content, log in to check access

Notes

Acknowledgment

We want to thank the members of our lab who contributed to several of the cited studies. Special thanks are due to Dr. Michael Reichert who gave helpful advice on the English style and substantially improved the manuscript, as well as to an anonymous reviewer whom we owe many helpful suggestions.

References

  1. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedGoogle Scholar
  2. Autrum HJ (1942) Schallempfang bei Mensch und Tier. Naturwissenschaften 5:69–85Google Scholar
  3. Barth FG (2002) A spider’s world: senses and behavior. Springer, Berlin/Heidelberg/New YorkGoogle Scholar
  4. Benda J, Hennig RM (2008) Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comput Neurosci 24:113–136PubMedGoogle Scholar
  5. Benda J, Herz AVM (2003) A universal model for spike-frequency adaptation. Neural Comput 15:2523–2564PubMedGoogle Scholar
  6. Bennet-Clark HC (1998) Size and scale effects as constraints in insect sound communication. Phil Trans R Soc Lond B 353:407–419Google Scholar
  7. Bentley DR, Hoy RR (1972) The genetic control of the neuronal network generating cricket (Teleogryllus gryllus) song pattern. Anim Behav 20:478–492PubMedGoogle Scholar
  8. Bernal XE, Rand AS, Ryan MJ (2006) Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to tungara frog calls. Behav Ecol 17:709–715Google Scholar
  9. Boyan GS, Fullard JH (1988) Information processing at a central synapse suggests a noise filter in the auditory pathway of the noctuid moth. J Comp Physiol A 164:251–258PubMedGoogle Scholar
  10. Brown CH (1994) Sound localization. In: Fay RR, Popper AN (eds) Comparative hearing: mammals. Springer, New York/Berlin, pp 57–96Google Scholar
  11. Brumm H, Slabbekoorn H (2005) Acoustic communication in noise. Adv Stud Behav 35:151–209Google Scholar
  12. Bura VL, Rower VG, Martin PR, Yack JE (2011) Whistling in caterpillars (Amorpha juglandis, Bombycoidea): sound-producing mechanism and function. J Exp Biol 214:30–37PubMedGoogle Scholar
  13. Bush SL, Schul J (2006) Pulse-rate recognition in an insect: evidence of a role for oscillatory neurons. J Comp Physiol A 192:113–121Google Scholar
  14. Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comput Neurosci 35:75–85PubMedGoogle Scholar
  15. Clemens J, Ronacher B (2013) Feature extraction and integration underlying perceptual decision making during courtship in grasshoppers. J Neurosci 33:12136–12145PubMedGoogle Scholar
  16. 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 108:13812–13817PubMedCentralPubMedGoogle Scholar
  17. Clemens J, Wohlgemuth S, Ronacher B (2012) Nonlinear computations underlying temporal and population sparseness in the auditory system of the grasshopper. J Neurosci 32:10053–10062PubMedGoogle Scholar
  18. Creutzig F, Wohlgemuth S, Stumpner A, Benda J, Ronacher B, Herz AVM (2009) Time-scale invariant representation of acoustic communication signals by a bursting neuron. J Neurosci 29:2575–2580PubMedGoogle Scholar
  19. Daugman JG (1984) Spatial visual channels in the Fourier plane. Vision Res 24:891–910PubMedGoogle Scholar
  20. de Boer E (1985) Auditory time constants: a paradox? In: Michelsen A (ed) Time resolution in auditory systems. Springer, Berlin/Heidelberg, pp 141–157Google Scholar
  21. Faure PA, Mason AC, Yack JE (2009) Invertebrate ears and hearing. In: Binder MD, Hirokawa N, Windhorst U, Hirsch MC (eds) Encyclopedia of neuroscience. Springer, Berlin, pp 2035–2042Google Scholar
  22. Franz A, Ronacher B (2002) Temperature dependence of temporal resolution in an insect nervous system. J Comp Physiol A 188:261–271Google Scholar
  23. Fullard JH, Yack JE (1993) The evolutionary biology of insect hearing. Trends Ecol Evol 8:248–252PubMedGoogle Scholar
  24. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, ChicagoGoogle Scholar
  25. Gollisch T, Herz AVM (2004) Input-driven components of spike-frequency adaptation can be unmasked in vivo. J Neurosci 24:7435–7444PubMedGoogle Scholar
  26. Gollisch T, Herz AVM (2005) Disentangling sub-millisecond processes within an auditory transduction chain. PLoS Biol 3(e8):1–11Google Scholar
  27. Green DM (1985) Temporal factors in psychoacoustics. In: Michelsen A (ed) Time resolution in auditory systems. Springer, Berlin/Heidelberg, pp 122–140Google Scholar
  28. Greenfield MD (1994) Synchronous and alternating choruses in insects and anurans: common mechanisms and diverse functions. Am Zool 34:605–615Google Scholar
  29. Greenfield MD, Roizen I (1993) Katydid synchronous chorusing is an evolutionary stable outcome of female choice. Nature 364:618–620Google Scholar
  30. Grothe B (2000) The evolution of temporal processing in the medial superior olive, an auditory brainstem structure. Prog Neurobiol 61:581–610PubMedGoogle Scholar
  31. Hartbauer M, Kratzer S, Steiner K, Römer H (2005) Mechanisms for synchrony and alternation in song interactions of the bushcricket Mecopoda elongata (Tettigoniidae, Orthoptera). J Comp Physiol A 191:175–188Google Scholar
  32. Hennig RM (2003) Acoustic feature extraction by cross-correlation in crickets? J Comp Physiol A 189:589–598Google Scholar
  33. 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 195:971–987Google Scholar
  34. Hennig RM, Franz A, Stumpner A (2004) Processing of auditory information in insects. Microsc Res Tech 63:351–374PubMedGoogle Scholar
  35. Hildebrandt KJ (2014) Neural maps in insect versus vertebrate auditory systems. Curr Opin Neurobiol 24:82–87PubMedGoogle Scholar
  36. Hildebrandt KJ, Benda J, Hennig RM (2009) The origin of adaptation in the auditory pathway of locusts is specific to cell type and function. J Neurosci 29:2626–2636PubMedGoogle Scholar
  37. Hildebrandt KJ, Benda J, Hennig RM (2011) Multiple arithmetic operations in a single neuron: the recruitment of adaptation processes in the cricket auditory pathway depends on sensory context. J Neurosci 31:14142–14150PubMedGoogle Scholar
  38. Hoy RR (1989) Startle, categorical response, and attention in acoustic behavior of insects. Ann Rev Neurosci 12:355–375PubMedGoogle Scholar
  39. Hoy RR, Popper AN, Fay RR (eds) (1998) Comparative hearing: insects. Springer, New YorkGoogle Scholar
  40. Huber F (1992) Verhalten und Neurobiologie von stimmbegabten Insekten. Naturwissenschaften 79:393–406Google Scholar
  41. Huber F, Markl H (1983) Neuroethology and behavioural physiology: roots and growing points. Springer, Heidelberg/New YorkGoogle Scholar
  42. Huber F, Moore TE, Loher W (eds) (1989) Cricket behavior and neurobiology. Cornell University Press, IthacaGoogle Scholar
  43. Hummel J, Kössl M, Nowotny M (2011) Sound-induced tympanal membrane motion in bushcrickets and its relationship to sensory output. J Exp Biol 214:3596–3604PubMedGoogle Scholar
  44. Janssen R (1992) Thermal influences on nervous system function. Neurosci Biobehav Rev 16:399–413PubMedGoogle Scholar
  45. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577PubMedGoogle Scholar
  46. Konishi M (1990) Similar algorithms in different sensory systems and animals. Cold Spring Harb Symp Quant Biol 55:575–584PubMedGoogle Scholar
  47. Kostarakos K, Hedwig B (2012) Calling song recognition in female crickets: temporal tuning of identified brain neurons matches behavior. J Neurosci 32:9601–9612Google Scholar
  48. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13–24PubMedGoogle Scholar
  49. Krahe R, Ronacher B (1993) Long rise times of sound pulses in grasshopper songs improve the directionality cues received by the CNS from auditory receptors. J Comp Physiol A 173:425–434Google Scholar
  50. Lakes-Harlan R, Stölting H, Stumpner A (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proc R Soc Lond B 266:1161–1167Google Scholar
  51. Lehmann GUC, Strauß J, Lakes-Harlan R (2007) Listening when there is no sexual signalling? Maintenance of hearing in the asexual bushcricket Poecilimon intermedius. J Comp Physiol A 193:537–545Google Scholar
  52. Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AVM (2001) Representation of acoustic communication signals by insect auditory receptor neurons. J Neurosci 21:3215–3227PubMedGoogle Scholar
  53. Machens CK, Schütze H, Franz A, Stemmler MB, Ronacher B, Herz AVM (2003) Auditory receptor neurons preserve characteristic differences between conspecific communication signals. Nat Neurosci 6:341–342PubMedGoogle Scholar
  54. Marquart V (1985) Local interneurons mediating excitation and inhibition onto ascending neurons in the auditory pathway of grasshoppers. Naturwissenschaften 72:42–44Google Scholar
  55. Marsat G, Pollack GS (2006) A behavioural role for feature detection by sensory bursts. J Neurosci 26:10542–10547PubMedGoogle Scholar
  56. McDonnell MD, Ward LM (2011) The benefits of noise in neural systems: bridging theory and experiment. Nat Rev Neurosci 12:415–425PubMedGoogle Scholar
  57. Meier T, Reichert H (1990) Embryonic development and evolutionary origin of the Orthopteran auditory organs. J Neurobiol 21:592–610PubMedGoogle Scholar
  58. Michelsen A (1979) Insect ears as mechanical systems. Am Sci 67:696–706Google Scholar
  59. Michelsen A (ed) (1985) Time resolution in auditory systems. Springer, Berlin/HeidelbergGoogle Scholar
  60. Michelsen A (1998) Biophysics of sound localization in insects. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, Berlin/New York, pp 18–62Google Scholar
  61. Michelsen A, Larsen ON (1983) Strategies for acoustic communication in complex environments. In: Huber F, Markl H (eds) Neuroethology and behavioural physiology. Springer, Berlin/Heidelberg, pp 321–331Google Scholar
  62. Michelsen A, Popov A, Lewis B (1994) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175:153–164Google Scholar
  63. Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. BioScience 51:571–582Google Scholar
  64. Moiseff A, Pollack G, Hoy R (1978) Steering responses of flying crickets to sound and ultrasound: mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056PubMedCentralPubMedGoogle Scholar
  65. Montealegre-Z F, Jonsson T, Robson-Brown KA, Postles M, Robert D (2012) Convergent evolution between insect and mammalian audition. Science 338:968–971PubMedGoogle Scholar
  66. Nadrowski B, Effertz T, Senthilan PR, Göpfert MC (2011) Antennal hearing in insects – new findings, new questions. Hearing Res 273:7–13Google Scholar
  67. 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 197:251–265Google Scholar
  68. Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: the role of behavioral context. Science 226:992–994PubMedGoogle Scholar
  69. Penzlin H (2005) Lehrbuch der Tierpyhsiologie. Elsevier, MünchenGoogle Scholar
  70. Pohl NU, Slabbekoorn H, Neubauer H, Heil P, Klump GM, Langemann U (2013) Why longer song elements are easier to detect: threshold level-duration functions in the Great Tit and comparison with human data. J Comp Physiol A 199:239–252Google Scholar
  71. Pollack GS (1988) Selective attention in an insect auditory neuron. J Neurosci 8:2635–2639PubMedGoogle Scholar
  72. Pollack GS, Hoy RR (1979) Temporal pattern as a cue for species-specific calling song recognition in crickets. Science 204:429–432PubMedGoogle Scholar
  73. Priebe NJ, Ferster D (2012) Mechanisms of neuronal computation in mammalian visual cortex. Neuron 75:194–208PubMedCentralPubMedGoogle Scholar
  74. Prinz P, Ronacher B (2002) Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.). J Comp Physiol A 188:577–587Google Scholar
  75. Riede K (1987) A comparative study of mating behaviour in some neotropical grasshoppers (Acridoidea). Ethology 76:265–296Google Scholar
  76. Riede K, Kämper G, Höfler I (1990) Tympana, auditory thresholds, and projection areas of tympanal nerves in singing and silent grasshoppers (Insects, Acridoidea). Zoomorphology 109:223–230Google Scholar
  77. Rieke F, Warland D, de Ruyter van Steveninck R, Bialek W (1997) Spikes – exploring the neural code. MIT Press, Cambridge, MAGoogle Scholar
  78. Robert D, Göpfert MC (2002) Novel schemes for hearing and orientation in insects. Curr Opin Neurobiol 12:715–720PubMedGoogle Scholar
  79. Robert D, Hoy RR (1998) The evolutionary innovation of tympanal hearing in Diptera. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, New York, pp 197–227Google Scholar
  80. Robert D, Miles RN, Hoy RR (1996) Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea. J Comp Physiol A 179:29–44PubMedGoogle Scholar
  81. Robertson RM, Money TG (2012) Temperature and neuronal circuit function: compensation, tuning and tolerance. Curr Opin Neurobiol 22:724–734PubMedGoogle Scholar
  82. Römer H (1976) Die Informationsverarbeitung tympanaler Rezeptorelemente von Locusta migratoria. J Comp Physiol A 109:101–122Google Scholar
  83. Römer H (1983) Tonotopic organization of the auditory neuropile in the bushcricket Tettigonia viridissima. Nature 306:60–62Google Scholar
  84. Römer H (2001) Ecological constraints for sound communication: from grasshoppers to elephants. In: Barth FG, Schmid A (eds) Ecology of sensing. Springer, Berlin/Heidelberg/New York, pp 59–77Google Scholar
  85. Römer H, Krusch M (2000) A gain-control mechanism for processing of chorus sounds in the afferent auditory pathway of the bushcricket Tettigonia viridissima (Orthoptera, Tettigoniidae). J Comp Physiol A 186:181–191PubMedGoogle Scholar
  86. Römer H, Lewald J (1992) High-frequency sound transmission in natural habitats: implications for the evolution of insect acoustic communication. Behav Ecol Sociobiol 29:437–444Google Scholar
  87. Römer H, Marquart V, Hardt M (1988) Organization of a sensory neuropile in the auditory pathway of two groups of Orthoptera. J Comp Neurol 275:201–215PubMedGoogle Scholar
  88. Römer H, Bailey WJ, Dadour I (1989) Insect hearing in the field: III masking by noise. J Comp Physiol A 164:609–620Google Scholar
  89. Römer H, Spickermann M, Bailey W (1998) Sensory basis for sound intensity discrimination in the bushcricket Requena verticalis (Tettigoniidae, Orthoptera). J Comp Physiol A 182:595–607Google Scholar
  90. Ronacher B (2013) Processing of species-specific signals in the auditory pathway of grasshoppers. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, Berlin, Heidelberg, pp. 185–204Google Scholar
  91. Ronacher B, Krahe R (2000) Temporal integration vs. parallel processing: coping with the variability of neuronal messages in directional hearing of insects. Eur J Neurosci 12:2147–2156PubMedGoogle Scholar
  92. Ronacher B, Stumpner A (1988) Filtering of behaviourally relevant temporal parameters of a grasshopper´s song by an auditory interneuron. J Comp Physiol A 163:517–523Google Scholar
  93. 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 158:363–374Google Scholar
  94. Ronacher B, Franz A, Wohlgemuth S, Hennig H (2004) Variability of spike trains and the processing of temporal patterns of acoustic signals–problems, constraints, and solutions. J Comp Physiol A 190:257–277Google Scholar
  95. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185Google Scholar
  96. Schildberger K (1994) The auditory pathway of crickets: adaptations for intraspecific acoustic communication. In: Schildberger K, Elsner N (eds) Neural basis of behavioural adaptations. G Fischer, Stuttgart, pp 209–225Google Scholar
  97. Schildberger K, Elsner N (1994) Neural basis of behavioural adaptations. G. Fischer, StuttgartGoogle Scholar
  98. 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 194:221–233Google Scholar
  99. Schmidt AKD, Riede K, Römer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762PubMedPubMedCentralGoogle Scholar
  100. Schneider E, Hennig RM (2012) Temporal resolution for calling song signals by female crickets, Gryllus bimaculatus. J Comp Physiol A 198:181–191Google Scholar
  101. Schul J, Sheridan RA (2006) Auditory stream segregation in an insect. Neuroscience 138:1–4PubMedGoogle Scholar
  102. Schul J, von Helversen D, Weber T (1998) Selective phonotaxis in Tettigonia cantans and T. viridissima in song recognition and discrimination. J Comp Physiol A182:687–694Google Scholar
  103. Selverston A, Kleindienst H-U, Huber F (1985) Synaptic connectivity between cricket auditory interneurons as studied by selective photoinactivation. J Neurosci 5:1283–1292PubMedGoogle Scholar
  104. Senthilan PR, Piepenbrock D, Ovezmyradov G, Nadrowski B, Bechstedt S, Pauls S, Winkler M, Möbius W, Howard J, Göpfert MC (2012) Drosophila auditory organ genes and genetic hearing defects. Cell 150:1042–1054PubMedGoogle Scholar
  105. Siegert ME, Römer H, Hashim R, Hartbauer M (2011) Neuronal correlates of a preference for leading signals in the synchronizing bushcricket Mecopoda elongata (Orthoptera: Tettigoniidae). J Exp Biol 214:3924–3934PubMedCentralPubMedGoogle Scholar
  106. Simoncelli E, Olshausen B (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216PubMedGoogle Scholar
  107. Smith EC, Lewicki MS (2006) Efficient auditory coding. Nature 439:978–982PubMedGoogle Scholar
  108. Stabel J, Wendler G, Scharstein H (1989) Cricket phonotaxis: localization depends on recognition of the calling song pattern. J Comp Physiol A 165:165–177Google Scholar
  109. Stölting H, Stumpner A (1998) Tonotopic organization of auditory receptors of the bushcricket Pholidoptera griseoaptera (Tettigoniidae, Decticinae). Cell Tissue Res 294:377–386PubMedGoogle Scholar
  110. Stumpner A (1996) Tonotopic organization of the hearing organ in a bushcricket. Naturwissenschaften 83:81–84Google Scholar
  111. Stumpner A (1997) An auditory interneurone tuned to the male song frequency in the duetting bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). J Exp Biol 200:1089–1101PubMedGoogle Scholar
  112. Stumpner A, Lakes-Harlan R (1996) Auditory interneurons in a hearing fly (Therobia leonidei, Ormiini, Tachinidae, Diptera). J Comp Physiol A 178:227–233Google Scholar
  113. Stumpner A, von Helversen D (2001) Evolution and function of auditory systems in insects. Naturwissenschaften 88:159–170PubMedGoogle Scholar
  114. Suga N, Zhang Y, Yan J (1997) Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. J Neurophysiol 77:2098–2114PubMedGoogle Scholar
  115. Tougaard J (1998) Detection of short pure-tone stimuli in the noctuid ear: what are temporal integration and integration time all about? J Comp Physiol A 183:563–572Google Scholar
  116. van Rossum MCW (2001) A novel spike distance. Neural Comput 13:751–763PubMedGoogle Scholar
  117. van Staaden MJ, Römer H (1998) Evolutionary transition from stretch to hearing organs in ancient grasshoppers. Nature 394:773–776Google Scholar
  118. Viemeister NF, Plack CJ (1993) Time analysis. In: Yost WA, Popper AN, Fay RR (eds) Human psychophysics. Springer, Berlin/Heidelberg/New York, pp 116–154Google Scholar
  119. Viemeister NF, Wakefield GH (1991) Temporal integration and multiple looks. J Acoust Soc Am 90:858–865PubMedGoogle Scholar
  120. Vogel A, Ronacher B (2007) Neural correlations increase between consecutive processing levels in the auditory system of locusts. J Neurophysiol 97:3376–3385PubMedGoogle Scholar
  121. Vogel A, Hennig RM, Ronacher B (2005) Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J Neurophysiol 93:3548–3559PubMedGoogle Scholar
  122. von Helversen D (1972) Gesang des Männchens und Lautschema des Weibchens bei der Feldheuschrecke Chorthippus biguttulus (Orthoptera, Acrididae). J Comp Physiol 81:381–422Google Scholar
  123. von Helversen D (1984) Parallel processing in auditory pattern recognition and directional analysis by the grasshopper Chorthippus biguttulus L (Acrididae). J Comp Physiol A 154:837–846Google Scholar
  124. von Helversen D (1997) Acoustic communication and orientation in grasshoppers. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser, Basel, pp 301–341Google Scholar
  125. von Helversen D, Rheinlaender (1988) Interaural intensity and time discrimination in an unrestrained grasshopper: a tentative behavioural approach. J Comp Physiol A 162:333–340Google Scholar
  126. von Helversen D, von Helversen O (1975a) Verhaltensgenetische Untersuchungen am akustischen Kommunikationssystem der Feldheuschrecken (Orthoptera, Acrididae). I. Der Gesang von Artbastarden zwischen Chorthippus biguttulus und C. mollis. J Comp Physiol 104:273–299Google Scholar
  127. von Helversen D, von Helversen O (1975b) Verhaltensgenetische Untersuchungen am akustischen Kommunikationssystem der Feldheuschrecken (Orthoptera, Acrididae). II. Das Lautschema von Artbastarden zwischen Chorthippus biguttulus und C. mollis. J Comp Physiol 104:301–323Google Scholar
  128. von Helversen D, von Helversen O (1995) Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing. J Comp Physiol A 177:767–774Google Scholar
  129. 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 180:373–386Google Scholar
  130. von Helversen D, von Helversen O (1998) Acoustic pattern recognition in a grasshopper: processing in the frequency or time domain? Biol Cybern 79:467–476Google Scholar
  131. von Helversen O, von Helversen D (1987) Innate receiver mechanisms in the acoustic communication of orthopteran insects. In: Guthrie DM (ed) Aims and methods in neuroethology. Manchester Univ Press, Manchester, pp 104–150Google Scholar
  132. 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
  133. Webb B, Wessnitzer J, Bush SL, Schul J, Buchli J, Ijspeert A (2007) Resonant neurons and bushcricket behaviour. J Comp Physiol A 193:285–288Google Scholar
  134. Weber T, Thorson J (1989) Phonotactic behavior of walking crickets. In: Huber F, Moore TE, Loher W (eds) Cricket behavior and neurobiology. Cornell University Press, Ithaca, pp 310–339Google Scholar
  135. Wendler G (1989) Acoustic orientation in crickets in the presence of two sound sources. Naturwissenschaften 76:128–129Google Scholar
  136. Wiley RH (2006) Signal detection and animal communication. Adv Study Behav 36:217–247Google Scholar
  137. Windmill JFG, Göpfert MC, Robert D (2005) Tympanal travelling waves in migratory locusts. J Exp Biol 208:157–168PubMedGoogle Scholar
  138. Wohlgemuth S, Ronacher B (2007) Auditory discrimination of amplitude modulations based on metric distances of spike trains. J Neurophysiol 97:3082–3092PubMedGoogle Scholar
  139. 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 197:61–74Google Scholar
  140. Yost WA (2000) Fundamentals of hearing – an introduction. Academic, San Diego/New YorkGoogle Scholar
  141. 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 105:2181–2194PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of BiologyHumboldt-Universität zu BerlinBerlinGermany