Journal of Comparative Physiology A

, Volume 196, Issue 4, pp 285–297 | Cite as

Intensity invariance properties of auditory neurons compared to the statistics of relevant natural signals in grasshoppers

  • Jan ClemensEmail author
  • Gerroth Weschke
  • Astrid Vogel
  • Bernhard Ronacher
Original Paper


The temporal pattern of amplitude modulations (AM) is often used to recognize acoustic objects. To identify objects reliably, intensity invariant representations have to be formed. We approached this problem within the auditory pathway of grasshoppers. We presented AM patterns modulated at different time scales and intensities. Metric space analysis of neuronal responses allowed us to determine how well, how invariantly, and at which time scales AM frequency is encoded. We find that in some neurons spike-count cues contribute substantially (20–60%) to the decoding of AM frequency at a single intensity. However, such cues are not robust when intensity varies. The general intensity invariance of the system is poor. However, there exists a range of AM frequencies around 83 Hz where intensity invariance of local interneurons is relatively high. In this range, natural communication signals exhibit much variation between species, suggesting an important behavioral role for this frequency band. We hypothesize, just as has been proposed for human speech, that the communication signals might have evolved to match the processing properties of the receivers. This contrasts with optimal coding theory, which postulates that neuronal systems are adapted to the statistics of the relevant signals.


Spike-train metric Decoding Acoustic communication Optimal coding Evolution 



We thank Matthias Hennig as well as the anonymous reviewers for helpful comments on previous versions of the manuscript and M. Bauer and O. von Helversen for providing the grasshopper song recordings. The study was supported by grants from the Bundesministerium für Bildung und Forschung (Bernstein Center for Computational Neuroscience) and the Deutsche Forschungsgemeinschaft (Sonderforschungsbereich 618) to B.R. The experiments comply with the current laws on “Principles of animal care” in Germany.


  1. Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275(5297):221–224CrossRefGoogle Scholar
  2. Arnqvist G (2006) Sensory exploitation and sexual conflict. Philos Trans R Soc Lond B Biol Sci 361(1466):375–386CrossRefPubMedGoogle Scholar
  3. Atick J (1992) Could information theory provide an ecological theory of sensory processing? Network 3(2):213–251CrossRefGoogle Scholar
  4. Attneave F (1954) Some informational aspects of visual perception. Psychol Rev 61(3):183–193CrossRefPubMedGoogle Scholar
  5. Barlow HB (1961) Possible principles underlying the transformations of sensory messages. In: Rosenblith WA (ed) Sensory communication. The MIT Press, Cambridge, pp 217–234Google Scholar
  6. Barlow HB (2001) Redundancy reduction revisited. Network 12(3):241–253PubMedGoogle Scholar
  7. Bauer M, von Helversen O (1987) Separate localization of sound recognizing and sound producing neural mechanisms in a grasshopper. J Comp Physiol A 161(1):95–101CrossRefGoogle Scholar
  8. Benda J, Hennig RM (2008) Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comput Neurosci 24(2):113–136CrossRefPubMedGoogle Scholar
  9. Benda J, Herz AV (2003) A universal model for spike-frequency adaptation. Neural Comput 15(11):2523–2564CrossRefPubMedGoogle Scholar
  10. Billimoria CP, Kraus BJ, Narayan R, Maddox RK, Sen K (2008) Invariance and sensitivity to intensity in neural discrimination of natural sounds. J Neurosci 28(25):6304–6308CrossRefPubMedGoogle Scholar
  11. Bridle JR, de La Bella JL, Butlin RK, Gosálvez J (2002) Low levels of chromosomal differentiation between the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (orthoptera; acrididae) in northern Spain. Genetica 114(2):121–127CrossRefPubMedGoogle Scholar
  12. Bugrov A, Novikova O, Mayorov V, Adkison L, Blinov A (2006) Molecular phylogeny of palaearctic genera of gomphocerinae grasshoppers (Orthoptera, Acrididae). Syst Entomol 31(2):362–368CrossRefGoogle Scholar
  13. Chander D, Chichilnisky EJ (2001) Adaptation to temporal contrast in primate and salamander retina. J Neurosci 21(24):9904–9916PubMedGoogle Scholar
  14. Creutzig F, Wohlgemuth S, Stumpner A, Benda J, Ronacher B, Herz AVM (2009) Timescale-invariant representation of acoustic communication signals by a bursting neuron. J Neurosci 29(8):2575–2580CrossRefPubMedGoogle Scholar
  15. Flook PK, Rowell CHF (1997) The phylogeny of the Caelifera (Insecta, Orthoptera) as deduced from mtrRNA gene sequences. Mol Phylogenet Evol 8(1):89–103CrossRefPubMedGoogle Scholar
  16. Franz A, Ronacher B (2002) Temperature dependence of temporal resolution in an insect nervous system. J Comp Physiol A 188(4):261–271CrossRefGoogle Scholar
  17. Gerhardt CH, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, LondonGoogle Scholar
  18. Guilford T, Dawkins MS (1993) Receiver psychology and the design of animal signals. Trends Neurosci 16(11):430–436CrossRefPubMedGoogle Scholar
  19. Hildebrandt JK, 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(8):2626–2636CrossRefPubMedGoogle Scholar
  20. Hoy RR, Hoikkala A, Kaneshiro K (1988) Hawaiian courtship songs: evolutionary innovation in communication signals of Drosophila. Science 240(4849):217–219CrossRefPubMedGoogle Scholar
  21. Joris PX, Schreiner CE, Rees A (2004) Neural processing of amplitude-modulated sounds. Physiol Rev 84(2):541–577CrossRefPubMedGoogle Scholar
  22. Koch C (1998) Biophysics of computation: information processing in single neurons (computational neuroscience). Oxford University Press, New YorkGoogle Scholar
  23. Kriegbaum H (1989) Female choice in the grasshopper Chorthippus biguttulus. Naturwissenschaften 76(2):81–82CrossRefGoogle Scholar
  24. Laughlin SB, Sejnowski TJ (2003) Communication in neuronal networks. Science 301(5641):1870–1874CrossRefPubMedGoogle Scholar
  25. Lawley DN, Maxwell AE (1971) Factor analysis as a statistical method, 2nd edn. Elsevier, New YorkGoogle Scholar
  26. Lewicki MS (2002) Efficient coding of natural sounds. Nat Neurosci 5(4):356–363CrossRefPubMedGoogle Scholar
  27. Lu T, Liang L, Wang X (2001) Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat Neurosci 4(11):1131–1138CrossRefPubMedGoogle Scholar
  28. Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AV (2001) Representation of acoustic communication signals by insect auditory receptor neurons. J Neurosci 21(9):3215–3227PubMedGoogle Scholar
  29. Machens CK, Schütze H, Franz A, Kolesnikova O, Stemmler MB, Ronacher B, Herz AV (2003) Single auditory neurons rapidly discriminate conspecific communication signals. Nat Neurosci 6(4):341–342CrossRefPubMedGoogle Scholar
  30. Machens CK, Wehr MS, Zador AM (2004) Linearity of cortical receptive fields measured with natural sounds. J Neurosci 24(5):1089–1100CrossRefPubMedGoogle Scholar
  31. Machens CK, Gollisch T, Kolesnikova O, Herz AV (2005) Testing the efficiency of sensory coding with optimal stimulus ensembles. Neuron 47(3):447–456CrossRefPubMedGoogle Scholar
  32. Martinez WL (2004) Exploratory data analysis with MATLAB (computer science and data analysis). Chapman and Hall/CRC, LondonGoogle Scholar
  33. Mendelson TC, Shaw KL (2005) Sexual behaviour: rapid speciation in an arthropod. Nature 433(7024):375–376CrossRefPubMedGoogle Scholar
  34. Narayan R, Grana G, Sen K (2006) Distinct time scales in cortical discrimination of natural sounds in songbirds. J Neurophysiol 96(1):252–258CrossRefPubMedGoogle Scholar
  35. Neuhofer D, Wohlgemuth S, Stumpner A, Ronacher B (2008) Evolutionarily conserved coding properties of auditory neurons across grasshopper species. Proc R Soc Lond B 208:1965–1974CrossRefGoogle Scholar
  36. Price T (1998) Sexual selection and natural selection in bird speciation. Philos Trans R Soc Lond B Biol Sci 353(1366):251–260CrossRefGoogle Scholar
  37. Rieke F, Warland D, van Steveninck R, Bialek W (1999) Spikes: exploring the neural code (computational neuroscience). The MIT Press, CambridgeGoogle Scholar
  38. Römer H (1987) Representation of auditory distance within a central neuropil of the bushcricket Mygalopsis marki. J Comp Physiol A 161(1):33–42CrossRefGoogle Scholar
  39. Römer H, Marquart V (1984) Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust. J Comp Physiol A 155(2):249–262CrossRefGoogle Scholar
  40. 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(2):201–215CrossRefPubMedGoogle Scholar
  41. 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(4):517–523CrossRefGoogle Scholar
  42. Ryan MJ, Phelps SM, Rand AS (2001) How evolutionary history shapes recognition mechanisms. Trends Cogn Sci 5(4):143–148CrossRefPubMedGoogle Scholar
  43. Sadagopan S, Wang X (2008) Level invariant representation of sounds by populations of neurons in primary auditory cortex. J Neurosci 28(13):3415–3426CrossRefPubMedGoogle Scholar
  44. Safi K, Heinzle J, Reinhold K (2006) Species recognition influences female mate preferences in the common european grasshopper (Chorthippus biguttulus Linnaeus, 1758. Ethology 112(12):1225–1230CrossRefGoogle Scholar
  45. Schmidt A, Ronacher B, Hennig R (2008) The role of frequency, phase and time for processing of amplitude modulated signals by grasshoppers. J Comp Physiol A 194(3):221–233CrossRefGoogle Scholar
  46. Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216CrossRefPubMedGoogle Scholar
  47. Smith EC, Lewicki MS (2006) Efficient auditory coding. Nature 439(7079):978–982CrossRefPubMedGoogle Scholar
  48. 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(1):391–410Google Scholar
  49. Stumpner A, Ronacher B (1994) Neurophysiological aspects of song pattern recognition and sound localization in grasshoppers. Am Zool 34(6):696–705Google Scholar
  50. Stumpner A, von Helversen D (2001) Evolution and function of auditory systems in insects. Naturwissenschaften 88(4):159–170CrossRefPubMedGoogle Scholar
  51. Stumpner A, Ronacher B, von Helversen O (1991) Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus: II. Processing of temporal patterns of the song of the male. J Exp Biol 158(1):411–430Google Scholar
  52. Theunissen F, Miller JP (1995) Temporal encoding in nervous systems: a rigorous definition. J Comput Neurosci 2(2):149–162CrossRefPubMedGoogle Scholar
  53. Uchida N, Mainen ZF (2007) Odor concentration invariance by chemical ratio coding. Front Syst Neurosci 1:3Google Scholar
  54. van Alphen JJM, Seehausen O, Galis F (2004) Speciation and radiation in African haplochromine cichlids. In: Diekmann U, Doebeli M, Metz JAJ, Tautz D (eds) Adaptive speciation (Cambridge studies in adaptive dynamics). Cambridge University Press, Cambridge, pp 54–75Google Scholar
  55. van Rossum MC (2001) A novel spike distance. Neural Comput 13(4):751–763CrossRefPubMedGoogle Scholar
  56. Vogel A, Ronacher B (2007) Neural correlations increase between consecutive processing levels in the auditory system of locusts. J Neurophysiol 97(5):3376–3385CrossRefPubMedGoogle Scholar
  57. Vogel A, Hennig RM, Ronacher B (2005) Increase of neuronal response variability at higher processing levels as revealed by simultaneous recordings. J Neurophysiol 93(6):3548–3559CrossRefPubMedGoogle Scholar
  58. von Helversen D (1972) Gesang des Männchens und Lautschema des Weibchens bei der Feldheuschrecke Chorthippus biguttulus (Orthoptera, Acrididae). J Comp Physiol A 81(4):381–422CrossRefGoogle Scholar
  59. 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(4):373–386CrossRefGoogle Scholar
  60. von Helversen D, von Helversen O (1998) Acoustic pattern recognition in a grasshopper: processing in the time or frequency domain? Biol Cybern 79(6):467–476CrossRefGoogle Scholar
  61. Wehner R (1987) ‘Matched filters’—neural models of the external world. J Comp Physiol A 161(4):511–531CrossRefGoogle Scholar
  62. 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(3):255–265CrossRefGoogle Scholar
  63. Wohlgemuth S, Ronacher B (2007) Auditory discrimination of amplitude modulations based on metric distances of spike trains. J Neurophysiol 97(4):3082–3092CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Jan Clemens
    • 1
    • 2
    Email author
  • Gerroth Weschke
    • 1
  • Astrid Vogel
    • 1
  • Bernhard Ronacher
    • 1
    • 2
  1. 1.Abteilung VerhaltensphysiologieInstitut für Biologie der Humboldt-Universität zu BerlinBerlinGermany
  2. 2.Bernstein Center for Computational Neuroscience BerlinBerlinGermany

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