Journal of Comparative Physiology A

, Volume 205, Issue 5, pp 717–733 | Cite as

Temporal processing properties of auditory DUM neurons in a bush-cricket

  • Andreas StumpnerEmail author
  • Paule Chloé Lefebvre
  • Marvin Seifert
  • Tim Daniel Ostrowski
Original Paper


Insects with ears process sounds and respond to conspecific signals or predator cues. Axons of auditory sensory cells terminate in mechanosensory neuropils from which auditory interneurons project into (brain-) areas to prepare response behaviors. In the prothoracic ganglion of a bush-cricket, a cluster of local DUM (dorsal unpaired median) neurons has recently been described and constitutes a filter bank for carrier frequency. Here, we demonstrate that these neurons also constitute a filter bank for temporal patterns. The majority of DUM neurons showed pronounced phasic-tonic responses. The transitions from phasic to tonic activation had different time constants in different DUM neurons. Time constants of the membrane potential were shorter in most DUM neurons than in auditory sensory neurons. Patterned stimuli with known behavioral relevance evoked a broad range of responses in DUM neurons: low-pass, band-pass, and high-pass characteristics were encountered. Temporal and carrier frequency processing were not correlated. Those DUM neurons producing action potentials showed divergent processing of temporal patterns when the graded potential or the spiking was analyzed separately. The extent of membrane potential fluctuations mimicking the patterned stimuli was different between otherwise similarly responding neurons. Different kinds of inhibition were apparent and their relevance for temporal processing is discussed.


Hearing Insect Temporal filtering Exponential fit Inhibition 



The project was funded by the German Science Foundation DFG STU 189/9-1 granted to AS. George Theophilidis, Aristotle University of Thessaloniki, Greece, helped with the permit to catch and export the insects. We thank Martin Göpfert for ongoing support. Heribert Gras gave numerous hints for using the Spike2 languages. Matthias Hennig initiated the use of intensity series of longer block stimuli for characterizing basic properties of temporal processing. We thank two anonymous reviewers for numerous helpful suggestions and Deborah Goggin (A.T. Still University) for meticulous proof reading and improving the English language.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

359_2019_1359_MOESM1_ESM.doc (1.6 mb)
Supplementary material 1 (DOC 1629 kb)


  1. Benda J, Hennig RM (2007) Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comput Neurosci 24:113–136CrossRefPubMedGoogle Scholar
  2. Benda J, Herz A (2003) A universal model for spike-frequency adaptation. Neural Comp 15:2523–2564CrossRefGoogle Scholar
  3. Bräunig P, Pflüger HJ (2001) The unpaired median neurons of insects. Adv Insect Physiol 28:185–266CrossRefGoogle Scholar
  4. Carr CE (1993) Processing of temporal information in the brain. Annu Rev Neurosci 16:223–243CrossRefPubMedGoogle Scholar
  5. Clemens J, Girardin CC, Coen P, Guan XJ, Dickson BJ, Murthy M (2015) Connecting neural codes with behavior in the auditory system of Drosophila. Neuron 87:1332–1343CrossRefPubMedPubMedCentralGoogle Scholar
  6. Clemens J, Ozeri-Engelhard N, Murthy M (2018) Fast intensity adaptation enhances the encoding of sound in Drosophila. Nat Commun 9:134CrossRefPubMedPubMedCentralGoogle Scholar
  7. Comer CM, Robertson RM (2001) Identified nerve cells and insect behavior. Prog Neurobiol 63:409–439CrossRefPubMedGoogle Scholar
  8. Dobler S, Heller K-G, von Helversen O (1994a) Song pattern recognition and an auditory time window in the female bush-cricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Comp Physiol A 175:67–74CrossRefGoogle Scholar
  9. Dobler S, Stumpner A, Heller K-G (1994b) Sex-specific spectral tuning for the partner’s song in the duetting bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Comp Physiol A 175:303–310Google Scholar
  10. Faure PA, Hoy RR (2000a) Neuroethology of the katydid T-cell. I. Tuning and responses to pure tones. J Exp Biol 203:3225–3242PubMedGoogle Scholar
  11. Faure PA, Hoy RR (2000b) Neuroethology of the katydid T-cell. II. Responses to acoustic playback of conspecific and predatory signals. J Exp Biol 203:3243–3254PubMedGoogle Scholar
  12. Feng AS, Hall JC, Siddique S (1991) Coding of temporal parameters of complex sounds by frog auditory nerve fibers. J Neurophysiol 65:424–445CrossRefPubMedGoogle Scholar
  13. Fielden A (1960) Transmission through the last abdominal ganglion of the dragonfly nymph, Anax imperator. J Exp Biol 37:832–844Google Scholar
  14. Galambos R, Davis H (1943) The response of single auditory-nerve fibers to acoustic stimulation. J Neurophysiol 6:39–57CrossRefGoogle Scholar
  15. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: Common problems and diverse solutions. Chicago University Press, ChicagoGoogle Scholar
  16. Gollisch T, Herz AVM (2004) Input-driven components of spike-frequency adaptation can be unmasked in vivo. J Neurosci 24:7435–7444CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gras H, Hörner M, Runge L, Schürmann FW (1990) Prothoracic DUM neurons of the cricket Gryllus bimaculatus: responses to natural stimuli and activity in walking behavior. J Comp Physiol A 166:901–914CrossRefGoogle Scholar
  18. Gustincich S, Feigenspan A, Wu DK, Koopman LJ, Raviola E (1997) Control of dopamine release in the retina: a transgenic approach to neural networks. Neuron 18:723–736CrossRefPubMedGoogle Scholar
  19. Hall JC (1994) Central processing of communication sounds in the anuran auditory system. Am Zool 34:670–684CrossRefGoogle Scholar
  20. Hedwig B (2014) Insect hearing and acoustic communication. Springer, NewYorkCrossRefGoogle Scholar
  21. Hedwig B (2016) Sequential filtering processes shape feature detection in crickets: a framework for song pattern recognition. Front Physiol 7:46CrossRefPubMedPubMedCentralGoogle Scholar
  22. Heller K-G, Hemp C, Ingrisch S, Liu C (2015) Acoustic communication in Phaneropterinae (Tettigonioidea): a global review with some new data. J Orthoptera Res 24:7–18CrossRefGoogle Scholar
  23. Heller K-G, von Helversen D (1986) Acoustic communication in phaneropterid bushcrickets: species-specific delay of female stridulatory response and matching male sensory time window. Behav Ecol Sociobiol 18:189–198CrossRefGoogle Scholar
  24. 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 29:2626–2636CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hildebrandt KJ, Benda J, Hennig RM (2015) Computational themes of peripheral processing in the auditory pathway of insects. J Comp Physiol A 201:39–50CrossRefGoogle Scholar
  26. Juusola M, French AS, Uusitalo RO, Weckström M (1996) Information processing by graded-potential transmission through tonically active synapses. Trends Neurosci 19:292–297CrossRefPubMedGoogle Scholar
  27. Kelly JB, Phillips DP (1991) Coding of interaural time differences of transients in auditory cortex of Rattus norvegicus: implications for the evolution of mammalian sound localization. Hear Res 55:39–44CrossRefPubMedGoogle Scholar
  28. Korsunovskaya O (2008) Acoustic signals in katydids (Orthoptera, Tettigonidae). Communication 1. Entomol Rev 88:1032–1050CrossRefGoogle Scholar
  29. Korsunovskaya O (2009) Acoustic signals in katydids (Orthoptera, Tettigonidae). Communication 2. Entomol Rev 89:16–20CrossRefGoogle Scholar
  30. Kretzberg J, Warzecha AK, Egelhaaf M (2001) Neural coding with graded membrane potential changes and spikes. J Comput Neurosci 11:153–164CrossRefPubMedGoogle Scholar
  31. Lai JS, Lo SJ, Dickson BJ, Chiang AS (2012) Auditory circuit in the Drosophila brain. Proc Natl Acad Sci U S A 109:2607–2612CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lang F, Brandt G, Glahe M (1993) A versatile multichannel acoustic stimulator controlled by a personal computer. In: Elsner N, Heisenberg M (eds) Gene, brain, behaviour. Thieme, Stuttgart, p A892Google Scholar
  33. Lefebvre PC, Seifert M, Stumpner A (2018) Auditory DUM neurons in a bush-cricket: a filter bank for carrier frequency. J Comp Neurol 526:1166–1182CrossRefPubMedGoogle Scholar
  34. Marquart V (1985) Auditorische Interneurone im thorakalen Nervensystem von Heuschrecken: Morphologie, Physiologie und synaptische Verbindungen. Dissertation, Universität BochumGoogle Scholar
  35. Mason AC, Faure PA (2004) The physiology of insect auditory afferents. Microsc Res Tech 63:338–350CrossRefPubMedGoogle Scholar
  36. Mason AC, Oshinsky ML, Hoy RR (2001) Hyperacute directional hearing in a microscale auditory system. Nature 410:686–690CrossRefPubMedGoogle Scholar
  37. Matsuo E, Seki H, Asai T, Morimoto T, Miyakawa H, Ito K, Kamikouchi A (2016) Organization of projection neurons and local neurons of the primary auditory center in the fruit fly Drosophila melanogaster. J Comp Neurol 524:1099–1164CrossRefPubMedGoogle Scholar
  38. Molina J, Stumpner A (2005) Effects of pharmacological treatment and photoinactivation on the directional responses of an insect neuron. J Exp Zool A 303:1085–1103CrossRefGoogle Scholar
  39. Montealegre-Z F (2009) Scale effects and constraints for sound production in katydids (Orthoptera: Tettigoniidae): correlated evolution between morphology and signal parameters. J Evol Biol 22:355–366CrossRefGoogle Scholar
  40. Ostrowski TD, Stumpner A (2010) Frequency processing at consecutive levels in the auditory system of bush crickets (Tettigoniidae). J Comp Neurol 518:3101–3116CrossRefPubMedGoogle Scholar
  41. Ostrowski TD, Stumpner A (2014) Response differences of intersegmental auditory neurons recorded close to or far away from the presumed spike-generating zone. J Comp Physiol A 200:627–639CrossRefGoogle Scholar
  42. Pollack GS (1994) Synaptic inputs to the omega neuron of the cricket Teleogryllus oceanicus: differences in EPSP waveforms evoked by low and high sound frequencies. J Comp Physiol A 174:83–89CrossRefGoogle Scholar
  43. Prešern J, Triblehorn JD, Schul J (2015) Dynamic dendritic compartmentalization underlies stimulus-specific adaptation in an insect neuron. J Neurophysiol 113:3787–3797CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rheinlaender J (1975) Transmission of acoustic information at three neuronal levels in the auditory system of Decticus verrucivorus (Tettigoniidae, Orthoptera). J Comp Physiol 97:1–53CrossRefGoogle Scholar
  45. Römer H, Dronse R (1982) Synaptic mechanisms of monaural and binaural processing in the locust. J Insect Physiol 28:365–370CrossRefGoogle Scholar
  46. Römer H, Seikowski U (1985) Responses to model songs of auditory neurons in the thoracic ganglia and brain of the locust. J Comp Physiol A 156:845–860CrossRefGoogle Scholar
  47. Römer H, Rheinlaender J, Dronse R (1981) Intracellular studies on auditory processing in the metathoracic ganglion of the locust. J Comp Physiol 144:305–312CrossRefGoogle Scholar
  48. Römer H, Marquart V, Hardt M (1988) The organization of a sensory neuropile in the auditory pathway of two groups of Orthoptera. J Comp Neurol 275:201–215CrossRefPubMedGoogle Scholar
  49. Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog. Science 219:1087–1089CrossRefPubMedGoogle Scholar
  50. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185CrossRefGoogle Scholar
  51. 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
  52. Schul J, Patterson AC (2003) What determines the tuning of hearing organs and the frequency of calls? A comparative study in the katydid genus Neoconocephalus (Orthoptera, Tettigoniidae). J Exp Biol 206:141–152CrossRefPubMedGoogle Scholar
  53. Schul J, von Helversen D, Weber T (1998) Selective phonotaxis in Tettigonia cantans and T. viridissima in song recognition and discrimination. J Comp Physiol A 182:687–694CrossRefGoogle Scholar
  54. 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. Springer, Berlin, pp 167–184Google Scholar
  55. Smith RL, Zwislocki JJ (1975) Short-term adaptation and incremental responses of single auditory-nerve fibers. Biol Cybern 17:169–182CrossRefPubMedGoogle Scholar
  56. Song H, Amédégnato C, Cigliano MM, Desutter-Grandcolas L, Heads SW, Huang Y, Otte D, Whiting WF (2015) 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics 31:621–651CrossRefGoogle Scholar
  57. Stabler SE, Palmer AR, Winter IM (1996) Temporal and mean rate discharge patterns of single units in the dorsal cochlear nucleus of the anesthetized guinea pig. J Neurophysiol 76:1667–1688CrossRefPubMedGoogle Scholar
  58. Stiedl O, Stumpner A, Mbungu D, Atkins G, Stout J (1997) Morphology and physiology of local auditory interneurons in the prothoracic ganglion of the cricket Acheta domesticus. J Exp Zool 279:43–53CrossRefGoogle Scholar
  59. Stritih N, Stumpner A (2009) Vibratory interneurons in the non-hearing cave cricket indicate evolutionary origin of sound processing elements in Ensifera. Zoology 112:48–68CrossRefPubMedGoogle Scholar
  60. 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
  61. Stumpner A (1998) Picrotoxin eliminates frequency selectivity of an auditory interneuron in a bushcricket. J Neurophysiol 79:2408–2415CrossRefPubMedGoogle Scholar
  62. Stumpner A (1999) An interneurone of unusual morphology is tuned to the female song frequency in the bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Exp Biol 202:2071–2081PubMedGoogle Scholar
  63. Stumpner A (2002) A species-specific frequency filter through specific inhibition, not specific excitation. J Comp Physiol A 188:239–248CrossRefGoogle Scholar
  64. Stumpner A, Meyer S (2001) Songs and the function of song elements in four duetting bushcricket species (Ensifera, Phaneropteridae, Barbitistes). J Insect Behav 14:511–533CrossRefGoogle Scholar
  65. Stumpner A, Molina J (2006) Diversity of intersegmental auditory neurons in a bush cricket. J Comp Physiol A 192:1359–1376CrossRefGoogle Scholar
  66. 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
  67. 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 158:411–430Google Scholar
  68. Stumpner A, Atkins G, Stout J (1995) Processing of unilateral and bilateral auditory inputs by the ON1 and L1 interneurons of the cricket Acheta domesticus and comparison to other cricket species. J Comp Physiol A 177:379–388CrossRefGoogle Scholar
  69. Sumner CJ, Palmer AR (2012) Auditory nerve fibre responses in the ferret. Eur J Neurosci 36:2428–2439CrossRefPubMedPubMedCentralGoogle Scholar
  70. Terzuolo CA, Washizu Y (1962) Relation between stimulus strength, generator potential and impulse frequency in stretch receptor of Crustacea. J Neurophysiol 25:56–66CrossRefPubMedGoogle Scholar
  71. Triblehorn JD, Schul J (2009) Sensory-encoding differences contribute to species-specific call recognition mechanisms. J Neurophysiol 102:1348–1357CrossRefPubMedPubMedCentralGoogle Scholar
  72. Triblehorn JD, Schul J (2013) Dendritic mechanisms contribute to stimulus-specific adaptation in an insect neuron. J Neurophysiol 110:2217–2226CrossRefPubMedPubMedCentralGoogle Scholar
  73. Vaughan AG, Zhou C, Manoli DS, Baker BS (2014) Neural pathways for the detection and discrimination of conspecific song in D. melanogaster. Curr Biol 24:1039–1049CrossRefPubMedGoogle Scholar
  74. Wildman MH, Cannone AJ (1990) Action potentials in a “non-spiking” neurone: graded responses and spikes in the afferent P fibre of the crab thoracic-coxal muscle receptor organ. Brain Res 509:339–342CrossRefPubMedGoogle Scholar
  75. Wohlers DW, Huber F (1978) Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L., Gryllus bimaculatus De Geer). J Comp Physiol A 127:11–28CrossRefGoogle Scholar
  76. Zimmermann U, Rheinlaender J, Robinson D (1989) Cues for male phonotaxis in the duetting bushcricket Leptophyes punctatissima. J Comp Physiol A 164:621–628CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department Cellular NeurobiologyUniversity of Göttingen, Johann-Friedrich-Blumenbach-Institute of Zoology and AnthropologyGöttingenGermany
  2. 2.ReugnyFrance
  3. 3.School of Life Science, Baden Lab for Vision and Visual EcologyUniversity of SussexFalmerUK
  4. 4.Kirksville College of Osteopathic MedicineA.T. Still UniversityKirksvilleUSA

Personalised recommendations