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Processing of Species-Specific Signals in the Auditory Pathway of Grasshoppers

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Insect Hearing and Acoustic Communication

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

Abstract

Species-specific acoustic signals of grasshoppers serve to attract mates; they are pivotal in avoiding hybridisation with sympatric species and to evaluate a potential mate’s quality. This necessitates a high precision of neuronal processing, which is constrained by the noisy nature of neuronal activity. Applying a spike train metric to estimate the variability of auditory responses, we quantified the respective impacts that external degradation of acoustic signals and intrinsic neuronal noise exert on signal processing. Unexpectedly, the variability of spike patterns increases from the afferents to the neurons whose axons ascend to the brain and reduces their ability to discriminate between similar communication signals. Between thoracic local and ascending neurons a change of coding principles seems to occur, leading to a population code with labelled-line characteristics. Thoracic auditory processing is conserved between distantly related species, suggesting that during evolution the communication signals have been adapted to match properties of the receiver’s sensory system.

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References

  • Arnqvist G (2006) Sensory exploitation and sexual conflict. Phil Trans R Soc Lond B 361:375–386

    Article  Google Scholar 

  • Barlow HB (1961) Possible principles underlying the transformations of sensory messages. In: Rosenblith WA (ed) Sensory communication. MIT Press, Cambridge, pp 217–234

    Google Scholar 

  • 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 

  • Berger D, Chobanov DP, Mayer F (2010) Interglacial refugia and range shifts of the alpine grasshopper Stenobothrus cotticus (Orthoptera: Acrididae: Gomphocerinae). Org Divers Evol 10:123–133

    Article  Google Scholar 

  • 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 

  • Brumm H, Slabbekoorn H (2005) Acoustic communication in noise. Adv Study Behav 35:151–209

    Article  Google Scholar 

  • Bugrov A, Novikova O, Mayorov V, Adkinson L, Blinov A (2006) Molecular phylogeny of Palaearctic genera of Gomphocerinae grasshoppers (Orthoptera, Acrididae). Syst Entomol 31:362–368

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Clemens J, Weschke G, Vogel A, Ronacher B (2010) Intensity invariance properties of auditory neurons compared to the statistics of relevant natural signals in grasshoppers. J Comp Physiol A 196:285–297

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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 29:2575–2580

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Einhäupl A, Stange N, Hennig RM, Ronacher B (2011) Attractiveness of grasshopper songs correlates with their robustness against noise. Behav Ecol 22:791–799

    Article  Google Scholar 

  • Elsner N (1974) Neuroethology of sound production in Gomphocerine grasshoppers (Orthoptera: Acrididae) 1. Song patterns and stridulatory movements. J Comp Physiol 88:67–102

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 

  • Franz A, Ronacher B (2002) Temperature dependence of temporal resolution in an insect nervous system. J Comp Physiol A 188:261–271

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Halex H, Kaiser W, Kalmring K (1988) Projection areas and branching patterns of the tympanal receptor cells in migratory locusts Locusta migratoria and Schistocerca gregaria. Cell Tissue Res 253:517–528

    Article  PubMed  CAS  Google Scholar 

  • Hedwig B (1992) On the control of stridulation in the acridid grasshopper Omocestus viridulus L. I Interneurons involved in rhythm generation and bilateral coordination. J Comp Physiol A 171:117–128

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Heller K-G (1988) Bioakustik der europäischen Laubheuschrecken. Josef Margraf Verlag, Weikersheim

    Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Houghton CJ, Sen K (2008) A new multineuron spike train metric. Neural Comput 20:1495–1511

    Article  PubMed  Google Scholar 

  • 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 

  • Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84:541–577

    Article  PubMed  CAS  Google Scholar 

  • Klappert K, Reinhold K (2003) Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus. Anim Behav 65:225–233

    Article  Google Scholar 

  • Klappert K, Reinhold K (2005) Local adaptation and sexual selection: a reciprocal transfer experiment with the grasshopper Chorthippus biguttulus. Behav Ecol Sociobiol 58:36–43

    Article  Google Scholar 

  • Kostarakos K, Römer H (2010) Sound transmission and directional hearing in field crickets: neurophysiological studies outdoors. J Comp Physiol A 196:669–681

    Article  Google Scholar 

  • Krahe R, Ronacher B (1993) Long rise times of sound pulses in grasshopper songs improve the directionality cues received by the CNS from the auditory receptors. J Comp Physiol A 173:425–434

    Article  Google Scholar 

  • Kriegbaum H (1989) Female choice in the grasshopper Chorthippus biguttulus: mating success is related to song characteristics of the male. Naturwissenschaften 76:81–82

    Article  Google Scholar 

  • Kriegbaum H, von Helversen O (1992) Influence of male songs on female mating behavior in the grasshopper Chorthippus biguttulus (Orthoptera, Acrididae). Ethology 91:248–254

    Article  Google Scholar 

  • Lang F (2000) Acoustic communication distances of a gomphocerine grasshopper. Bioacoustics 10:233–258

    Article  Google Scholar 

  • Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60:1799–1821

    CAS  Google Scholar 

  • 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 21:3215–3227

    PubMed  CAS  Google Scholar 

  • Machens CK, Schütze H, Franz A, Stemmler MB, Ronacher B, Herz AVM (2003) Auditory receptor neurons preserve characteristic differences between conspecific communication signals. Nature Neurosci 6:341–342

    Article  PubMed  CAS  Google Scholar 

  • Machens CK, Gollisch T, Kolesnikova O, Herz AVM (2005) Testing the efficiency of sensory coding with optimal stimulus ensembles. Neuron 47:447–456

    Article  PubMed  CAS  Google Scholar 

  • Marquart V (1985) Local interneurons mediating excitation and inhibition onto ascending neurons in the auditory pathway of grasshoppers. Naturwissensch 72:42–43

    Article  Google Scholar 

  • Mayer F, Berger D, Gottsberger B, Schulze W (2010) Non-Ecological radiations in acoustically communicating grasshoppers? In: Glaubrecht M (ed) Evolution in action. Springer, Berlin Heidelberg, pp 451–464

    Chapter  Google Scholar 

  • 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 

  • Michelsen A (1971) The physiology of the locust ear. I. Frequency selectivity of single cells in the isolated ear. Z vergl Physiol 71:49–62

    Article  Google Scholar 

  • Michelsen A, Larsen ON (1983) Strategies for acoustic communication in complex environments. In: Huber F, Markl H (eds) Neuroethology and behavioural physiology. Springer, Berlin, pp 321–331

    Google Scholar 

  • Mitchell M (1998) An introduction to genetic algorithms. MIT press, Boston

    Google Scholar 

  • Neuhofer D, Wohlgemuth S, Stumpner A, Ronacher B (2008) Evolutionarily conserved coding properties of auditory neurons across grasshopper species. Proc R Soc Lond B 208:1965–1974

    Article  Google Scholar 

  • 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 

  • Prinz P, Ronacher B (2002) Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.). J Comp Physiol A 188:577–587

    Article  CAS  Google Scholar 

  • Rokem A, Watzl S, Gollisch T, Stemmler MB, Herz AVM, Samengo I (2006) Spike-timing precision underlies the coding efficiency of auditory receptor neurons. J Neurophysiol 95:2541–2552

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Römer H (2001) Ecological constraints for sound communication: from grasshoppers to elephants. In: Barth FG, Schmid A (eds) Ecology of sensing. Springer, Berlin, pp 59–77

    Chapter  Google Scholar 

  • 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 

  • Römer H, Marquart V, Hardt M (1988) Organization of a sensory neuropile in the auditory pathway of two groups of Orthoptera. J Comp Neurol 275:201–215

    Article  PubMed  Google Scholar 

  • Ronacher B, Stange N (2012) Processing of acoustic signals in grasshoppers – a neuroethological approach towards female choice. J Physiol Paris 107:41–50

    Google Scholar 

  • 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 

  • 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 

  • Ronacher B, Franz A, Wohlgemuth S, Hennig RM (2004) Variability of spike trains and the processing of temporal patterns of acoustic signals – problems, constraints, and solutions. J Comp Physiol A 190:257–277

    Article  CAS  Google Scholar 

  • Ronacher B, Wohlgemuth S, Vogel A, Krahe R (2008) Discrimination of acoustic communication signals by grasshoppers: temporal resolution, temporal integration, and the impact of intrinsic noise. J Comp Psychol 22:252–263

    Article  Google Scholar 

  • Ryan MJ, Phelps SM, Rand AS (2001) How evolutionary history shapes recognition mechanisms. Trends Cogn Sci 5:143–148

    Google Scholar 

  • 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 209–225

    Google Scholar 

  • Schmidt AKD, Römer H (2011) Solutions to the cocktail party problem in insects: selective filters, spatial release from masking and gain control in tropical crickets. PLoS ONE 6:e 28593

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216

    Article  PubMed  CAS  Google Scholar 

  • Stange N, Ronacher B (2012) Grasshopper calling songs convey information about condition and health of males. J Comp Physiol A 198:309–318

    Article  Google Scholar 

  • Stumpner A (1988) Auditorische thorakale Interneurone von Chorthippus biguttulus L.: morphologische und physiologische Charakterisierung und Darstellung ihrer Filtereigenschaften für verhaltensrelevante Lautattrappen. Ph.D. thesis, Friedrich-Alexander Universität Erlangen-Nürnberg

    Google Scholar 

  • Stumpner A (1989) Physiological variability of auditory neurons in a grasshopper. Naturwissenschaften 76:427–429

    Article  Google Scholar 

  • Stumpner A, Molina J (2006) Diversity of intersegmental auditory neurons in a bush cricket. J Comp Physiol A 192:1359–1376

    Article  Google Scholar 

  • Stumpner A, Ronacher B (1991) Auditory interneurons in the metathoracic ganglion of the grasshopper Chorthippus biguttulus. 1. Morphological and physiological characterization. J Exp Biol 158:391–410

    Google Scholar 

  • Stumpner A, von Helversen O (1992) Recognition of a two-element song in the grasshopper Chorthippus dorsatus (Orthoptera: Gomphocerinae). J Comp Physiol A 171:405–412

    Article  Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • Stumpner A, Ronacher B, von Helversen O (1991) Auditory interneurons 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 

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

    Article  PubMed  CAS  Google Scholar 

  • van Rossum MCW (2001) A novel spike distance. Neural Comput 13:751–763

    Article  PubMed  Google Scholar 

  • Vedenina VY, Panyutin AK, von Helversen O (2007) The unusual inheritance pattern of the courtship songs in closely related grasshopper species of the Chorthippus albomarginatus-group (Orthoptera: Gomphocerinae). J Evol Biol 20:260–277

    Article  PubMed  Google Scholar 

  • Viemeister NF, Plack CJ (1993) Time analysis. In: Yost WA, Popper AN, Fay RR (eds) Human psychophysics. Springer, Berlin, pp 116–154

    Chapter  Google Scholar 

  • Vogel A, Ronacher B (2007) Neural correlations increase between consecutive processing levels in the auditory system of locusts. J Neurophysiol 97:3376–3385

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • von Helversen O (1979) Angeborenes Erkennen akustischer Schlüsselreize. Verh Deutsch Zool Ges 1979:42–59

    Google Scholar 

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

    Google Scholar 

  • 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 104:273–299

    Article  Google Scholar 

  • 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 104:301–323

    Article  Google Scholar 

  • 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 Verlag Stuttgart, pp 253–284

    Google Scholar 

  • 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 

  • 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 

  • Weschke G, Ronacher B (2008) Influence of sound pressure level on the processing of amplitude modulations by auditory neurons of the locust. J Comp Physiol A 194:255–265

    Article  Google Scholar 

  • White JA, Rubinstein JT, Kay AR (2000) Channel noise in neurons. Trends Neurosci 23:131–137

    Article  PubMed  CAS  Google Scholar 

  • Wohlers D, 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 

  • Wohlgemuth S (2008) Repräsentation und Unterscheidbarkeit amplitudenmodulierter akustischer Signale im Nervensystem von Feldheuschrecken. PhD thesis Humboldt- Universität zu Berlin

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 

  • Zador A (1998) Impact of synaptic unreliability on the information transmitted by spiking neurons. J Neurophysiol 79:1219–1229

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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Acknowledgements

I thank all members of my lab who contributed to the work reported here, in particular Matthias Hennig for years of fruitful collaboration and many stimulating discussions. I also thank Daniela Neuhofer, Jana Sträter, Astrid Vogel and Sandra Wohlgemuth for providing partially unpublished data. Special thanks to Stefanie Krämer for making the figures. Berthold Hedwig and Carl Gerhardt gave valuable suggestions that helped to improve the manuscript. The American Psychological Association, the Royal Society, and Springer Science and Business Media very kindly allowed the reproduction of figures. Financial support from the German Research Council (SFB 618, GRK 837, GRK 1589/1) and the Bernstein Centre for Computational Neuroscience (Federal Ministry of Education and Research, Germany, grant 01GQ1001A) is also gratefully acknowledged.

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Ronacher, B. (2014). Processing of Species-Specific Signals in the Auditory Pathway of Grasshoppers. 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_11

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