Computational themes of peripheral processing in the auditory pathway of insects

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 201, Issue 1, 2015, Pages 39-50

  Hildebrandt, K Jannis ^a   Benda, Jan ^b   Hennig, R Matthias ^c  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Neural coding; Sensory processing; Spike frequency adaptation

Indexed keywords

ANIMAL; AUDITORY NERVOUS SYSTEM; BIOLOGICAL MODEL; HEARING; INSECT; NERVE CELL; PHYSIOLOGY;

ANIMALS; AUDITORY PATHWAYS; HEARING; INSECTS; MODELS, NEUROLOGICAL; NEURONS;

EID: 84920457007     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-014-0956-5     Document Type: Review

References (91)

1. Autrum HJ (1942) Schallempfang bei mensch und tier. Naturwissenschaften 5:69–85
2. 2+ dynamics underlying sound processing in an auditory interneurone. Dev Neurobiol 67(1):68–80
3. Barlow HB (2001) Redundancy reduction revisited. Network 12(3):241–253
4. Benda J, Hennig RM (2008) Spike-frequency adaptation generates intensity invariance in a primary auditory interneuron. J Comput Neurosci 24:113–136
5. Benda J, Herz AVM (2003) A universal model for spike-frequency adaptation. Neural Comput 15:2523–2564
6. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland
7. Clemens J, Hennig RM (2013) Computational principles underlying the recognition of acoustic signals in insects. J Comput Neurosci 35:75–85
8. Clemens J, Ronacher B (2013) Feature extraction and integration underlying perceptual decision making during courtship behavior. J Neurosci 33(29):12136–12145
9. Clemens J, Weschke G, Vogel A, Ronacher B (2010) Intensity properties of auditory neurons compared to the statistics of relevant natural signals in grasshoppers. J Comp Physiol A 196:285–297
10. 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
11. 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
12. Creutzig F, Wohlgemuth S, Stumpner A, Bena J, Ronacher B, Herz AVM (2009) Time-scale invariant representation of acoustic communication signals by a bursting interneuron. J Neurosci 29:2575–2580
13. Creutzig F, Benda J, Wohlgemuth S, Stumpner A, Ronacher B, Herz AVM (2010) Timescale-invariant pattern recognition by feedforward inhibition and parallel signal processing. Neural Comput 22:1493–1510
14. deWeese MR, Wehr M, Zador AM (2003) Binary spiking in auditory cortex. J Neurosci 23(7940):7949
15. Dobler S, Stumpner A, Heller K-G (1994) Sex-specific spectral tuning for the partner’s song in the duetting bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Comp Physiol A 175:303–310
16. Eyherabide HG, Rokem A, Herz AVM, Samengo I (2008) Burst firing is a neural code in an insect auditory system. Front Comput Neurosci 2:1–17
17. Fisch K, Schwalger T, Lindner B, Herz AV, Benda J (2012) Channel noise from both slow adaptation currents and fast currents is required to explain spike-response variability in a sensory neuron. J Neurosci 32(48):17332–17344
18. Fonseca PJ, Münch D, Hennig RM (2000) How cicadas interpret acoustic signals. Nature 405:297–298
19. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans. University of Chicago Press, Chicago
20. Gogala M (1995) Songs of four cicada species from Thailand. Bioacoustics 6:101–116
21. Gollisch T, Herz AVM (2004) Input-driven components of spike-frequency adaptation can be unmasked in vivo. J Neurosci 24:7435–7444
22. 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
23. Hennig RM, Franz A, Stumpner A (2004) Processing of auditory information in insects. Microsc Res Tech 63:351–374
24. Hildebrandt KJ (2014) Neural maps in insect versus vertebrate auditory systems. Curr Opin Neurobiol 24:82–87
25. 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 29:2626–2636
26. 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 31:14142–14150
27. Hill KG (1974) Carrier frequency as a factor in phonotactic behavior of female crickets (Teleogryllus commodus). J Comp Physiol 93:7–18
28. Hoy RR (1989) Startle, categorical response, and attention in acoustic behavior of insects. Ann Rev Neurosci 12:355–375
29. Imaizumi K, Pollack GS (1999) Neural coding of sound frequency by cricket auditory receptors. J Neurosci 19:1508–1516
30. 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
31. Klump GM, Shelter MD (1984) Acoustic behaviour of birds and mammals in the predator context; I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm signals. Z Tierpsychol 66:189–226
32. 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
33. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13–24
34. Lampe U, Schmoll T, Franzke A, Reinhold K (2012) Staying tuned: grasshoppers from noisy roadside habitats produce courtship signals with elevated frequency components. Function Ecol 26:1348–1354
35. Laughlin SB (1981) A simple coding procedure enhances a neuron’s information capacity. Z Naturforsch C: Biosci 36:910–912
36. Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884–895
37. 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
38. 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
39. Machens CK, Gollisch T, Kolesnikova O, Herz AVM (2005) Testing the efficiency of sensory coding with optimal stimulus ensembles. Neuron 47:447–456
40. Marsat G, Pollack GS (2005) Effect of the temporal pattern of contralateral inhibition on sound localization cues. J Neurosci 25:6137–6144
41. Marsat G, Pollack GS (2006) A behavioral role for feature detection by sensory bursts. J Neurosci 26(41):10542–10547
42. Marsat G, Pollack GS (2010) The structure and size of sensory bursts encode stimulus information but only size affects behavior. J Comp Physiol A 196:315–320
43. Marshall DC, Hill KBR (2009) Versatile aggressive mimicry of cicadas by an Australian predatory katydid. PLoS One 4(1):e4185. doi:10.1371/journal.pone.0004185
44. Michelsen A (1998) Biophysics of sound localization in insects. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, Berlin, NewYork, pp 18–62
45. Miles RN, Robert D, Hoy RR (1995) Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea. J Acoust Soc Am 98:3059–3070
46. Neuhofer D, Ronacher B (2012) Influence of different envelope maskers on signal recognition and neuronal representation in the auditory system of a grasshopper. PLoS One 7(3):e34384
47. Neuhofer D, Wohlgemuth S, Stumpner A, Ronacher B (2008) Evolutionarily conserved coding properties of auditory across grasshopper species. Proc R Soc B 275:1965–1974
48. 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
49. Oldfield BP, Kleindienst H, Huber F (1986) Physiology and tonotopic organization of auditory receptors in the cricket Gryllus bimaculatus deGeer. J Comp Physiol A 159:457–464
50. Pollack GS (1988) Selective attention in an insect auditory neuron. J Neurosci 8:2635–2639
51. Poulet JFA, Hedwig B (2005) Auditory orientation in crickets: pattern recognition controls reactive steering. PNAS 102:15665–15669
52. Rokem A, Watzl S, Gollisch T, Stemmler M, Herz AVM, Samengo I (2006) Spike-timing precision underlies the coding efficiency of auditory receptor neurons. J Neurophysiol 95:2541–2552
53. Römer H (1987) Representation of auditory distance with a central neuropil of the bushcricket Megalopsis marki. J Comp Physiol 161:33–42
54. 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 186:181–191
55. Römer H, Lewald J (1992) High-frequency sound transmission in natural habitats: implications for the evolution of insect acoustic communication. Behav Ecol Sociobiol 29:437–444
56. Römer H, Bailey WJ, Dadour I (1989) Insect hearing in the field: III masking by noise. J Comp Physiol A 164:609–620
57. Römer H, Spickermann M, Bailey W (1998) Sensory basis for sound intensity discrimination in the bushcricket Requena verticalis (Tettigoniidae, Orthoptera). J Comp Physiol A 182:595–607
58. Römer H, Hedwig B, Ott SR (2002) Contralateral inhibition as a sensory bias: the neural basis for a female preference in a synchronously calling bushcricket, Mecopoda elongate. Eur J Neurosci 15:1655–1662
59. Ronacher B, Hennig RM (2004) Neuronal adaptation improves the recognition of temporal patterns in a grasshopper. J Comp Physiol A 190:311–319. doi:10.1007/s00359-004-0498-3
60. 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
61. Ronacher B, Stumpner A (1993) Parallel processing of song pattern and sound direction by ascending auditory interneurons in the grasshopper Chorthippus biguttulus. In: Wiese K, Gribakin FG, Popov AV, Renninger G (eds). Sensory systems of Arthropods. Birkhäuser, Basel, pp 376
62. 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
63. 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
64. Ronacher B, Hennig RM, Clemens J (2014) Computational principles underlying recognition of acoustic signals in grasshoppers and crickets. J Comp Physiol A. doi:10.1007/s00359-014-0946-7
65. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket’s brain. J Comp Physiol A 155:171–185
66. Schmidt AKD, Riede K, Römer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762
67. Schneider E, Hennig RM (2012) Temporal resolution for calling song signals by female crickets, Gryllus bimaculatus. J Comp Physiol A 198:181–191
68. Schul J, Sheridan RA (2006) Auditory stream segregation in an insect. Neuroscience 138:1–4
69. Schul J, von Helversen D, Weber T (1998) Selective phonotaxis in Tettigonia cantans and T. viridissima in song recognition and discrimination. J Comp Physiol A182:687–694
70. +dynamics in a cricket auditory neuron: an example of chemical computation. Science 263:823–826
71. Stabel J, Wendler G, Scharstein H (1989) Cricket phonotaxis: localization depends on recognition of the calling song pattern. J Comp Physiol A 165:165–177
72. Stumpner A (1997) An auditory interneurone tuned to the male song frequency in the duetting bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). J Exp Biol 200:1089–1101
73. Stumpner A (2002) A species-specific frequency filter through specific inhibition, not specific excitation. J Comp Physiol A 188:239–248
74. Stumpner A, Nowotny M (2014) Neural processing in the bushcricket auditory pathway. In: Hedwig B (ed) Topics of acoustic communication in insects, vol 1. Springer, Berlin, pp 143–166
75. 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
76. Stumpner A, Ronacher B (1994) Neurophysiological aspects of song pattern recognition and sound localization in grasshoppers. Am Zool 34:696–705
77. Stumpner A, von Helversen D (2001) Evolution and function of auditory systems in insects. Naturwissenschaften 88:159–170
78. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273–1276
79. Vogel A, Ronacher B (2007) Neural correlations increase between consecutive processing levels in the auditory system of locusts. J Neurophysiol 97:3376–3385
80. 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
81. 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
82. von Helversen D, von Helversen O (1995) Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing. J Comp Physiol A 177:767–774
83. 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
84. von Helversen D, von Helversen O (1998) Acoustic pattern recognition in a grasshopper: processing in the time or frequency domain? Biol Cybern 79(6):467–476
85. Vonderschen K, Chacron MJ (2011) Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish. J Neurophysiol 106:3102–3118
86. Wimmer K, Hildebrandt KJ, Hennig RM, Obermayer K (2008) Adaptation and selective information transmission in the cricket auditory neuron AN2. PLoS Comput Biol 4:e1000182. doi:10.1371/journal.pcbi.1000182
87. 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 146:161–173
88. Wohlgemuth S, Ronacher B (2007) Auditory discrimination of amplitude modulations based on metric distances of spike trains. J Neurophysiol 97:3082–3092
89. 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
90. Wyttenbach RA, May ML, Hoy RR (1996) Categorical perception of sound frequency by crickets. Science 273:1542–1544
91. Zorovic 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(5):2181–2194