Processing of auditory information in insects

Insects exhibit an astonishing diversity in the design of their ears and the subsequent processing of information within their auditory pathways. The aim of this review is to summarize and compare the present concepts of auditory processing by relating behavioral performance to known neuronal mechanisms. We focus on three general aspects, that is frequency, directional, and temporal processing. The first part compares the capacity (in some insects high) for frequency analysis in the ear with the rather low specificity of tuning in interneurons by looking at Q10dB values and frequency dependent inhibition of interneurons. Since sharpening of frequency does not seem to be the prime task of a set of differently tuned receptors, alternative hypotheses are discussed. Moreover, the physiological correspondence between tonotopic projections of receptors and dendritic organization of interneurons is not in all cases strong. The second part is concerned with directional hearing and thus with the ability for angular resolution of insects. The present concepts, as derived from behavioral performances, for angular resolution versus lateralization and serial versus parallel processing of directional and pattern information can be traced to the thoracic level of neuronal processing. Contralateral inhibition, a mechanism for enhancing directional tuning, appears to be most effective in parallel pathways, whereas in serial processing it may have detrimental effects on pattern processing. The third part, after some considerations of signal analysis in the temporal domain, demonstrates that closely related species often use different combinations of temporal parameters in their recognition systems. On the thoracic level, analysis of temporal modulation functions and effects of inhibition on spiking patterns reveals relatively simple processing, whereas brain neurons may exhibit more complex properties. Microsc. Res. Tech. 63:351–374, 2004. © 2004 Wiley‐Liss, Inc.

[1]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[2]  P. C. Wang,et al.  Specific phosphorylation of membrane proteins of Mr 44,000 and Mr 32,000 by the autophosphorylated insulin receptor from the hepatopancreas of the shrimp Penaeus monodon (Crustacea: Decapoda). , 1993, The Journal of experimental zoology.

[3]  R. Hoy,et al.  Neuroethology of the katydid T-cell. I. Tuning and responses to pure tones. , 2000, The Journal of experimental biology.

[4]  G. Jacobs,et al.  Neural Mapping of Direction and Frequency in the Cricket Cercal Sensory System , 1999, The Journal of Neuroscience.

[5]  Changes in phonotaxis by the female cricketAcheta domesticus L. after killing identified acoustic interneurons , 1984, Journal of Comparative Physiology A.

[6]  Franz Huber,et al.  Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L.,Gryllus bimaculatus DeGeer) , 1978, Journal of comparative physiology.

[7]  Axel Michelsen,et al.  Auditory Processing of Temporal Cues in Insect Songs: Frequency Domain or Time Domain? , 1985 .

[8]  A. Stumpner Tonotopic organization of the hearing organ in a bushcricket , 1996, Naturwissenschaften.

[9]  W. Rössler,et al.  Causes of the differences in detection of low frequencies in the auditory receptor organs of two species of bushcrickets , 1995 .

[10]  P. Brodfuehrer,et al.  Ultrasound sensitive neurons in the cricket brain , 1990, Journal of Comparative Physiology A.

[11]  A. Watson,et al.  Distribution of input and output synapses on the central branches of bushcricket and cricket auditory afferent neurones: Immunocytochemical evidence for GABA and glutamate in different populations of presynaptic boutons , 1999, The Journal of comparative neurology.

[12]  R. Seifert Raumorientierung und Phototaxis der Anostraken Euphyllopoden , 1932, Zeitschrift für vergleichende Physiologie.

[13]  B. Oldfield,et al.  Accuracy of orientation in female crickets,Teleogryllus oceanicus (Gryllidae): dependence on song spectrum , 1980, Journal of comparative physiology.

[14]  B. Ronacher,et al.  Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus. I, Morphological and physiological characterization , 1991 .

[15]  M. Hörner,et al.  The function of auditory neurons in cricket phonotaxis , 1988, Journal of Comparative Physiology A.

[16]  A. Surlykke Hearing in Notodontid Moths: a Tympanic Organ with a Single Auditory Neurone , 1984 .

[17]  J. Fullard The tuning of moth ears , 1988, Experientia.

[18]  M. Burrows Effects of temperan a central synapse between identified motor neurons in the locust , 1989, Journal of Comparative Physiology A.

[19]  Franz Huber,et al.  Acoustic Communication in Periodical Cicadas: Neuronal Responses to Songs of Sympatric Species , 1990 .

[20]  K. D. Roeder Interneurons of the thoracic nerve cord activated by tympanic nerve fibres in noctuid moths. , 1966, Journal of insect physiology.

[21]  R. M. Hennig Ascending auditory interneurons in the cricketTeleogryllus commodus (Walker): comparative physiology and direct connections with afferents , 1988, Journal of Comparative Physiology A.

[22]  Brian C. J. Moore,et al.  Across-channel processes in auditory masking , 1992 .

[23]  B. Grothe Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat. , 1994, Journal of neurophysiology.

[24]  Influence of syllable period on song encoding properties of an ascending auditory interneuron in the cricketAcheta domestica , 1989, Journal of Comparative Physiology A.

[25]  Acoustic Cues for Sound Localisation and Spacing in Orthopteran Insects , 1990 .

[26]  J. Rheinlaender,et al.  Electrical stimulation of the tympanal nerve as a tool for analysing the responses of auditory interneurons in the locust , 1983, Journal of comparative physiology.

[27]  R M Hennig,et al.  Auditory perception: How cicadas interpret acoustic signals , 2000, Nature.

[28]  A. Stumpner,et al.  Sex-specific spectral tuning for the partner's song in the duetting bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae) , 1994, Journal of Comparative Physiology A.

[29]  Auditory interneurons in Cyphoderris monstrosa (Orthoptera: Haglidae) , 2004, Journal of Comparative Physiology A.

[30]  The central acoustic tract and audio‐vocal coupling in the horseshoe bat, Rhinolophus rouxi , 2000, The European journal of neuroscience.

[31]  D. von Helversen,et al.  Acoustic communication and orientation in grasshoppers , 1997 .

[32]  Morphology and physiology of auditory and vibratory ascending interneurones in bushcrickets. , 2000, The Journal of experimental zoology.

[33]  F. Huber,et al.  Physiology and tonotopic organization of auditory receptors in the cricketGryllus bimaculatus DeGeer , 1986, Journal of Comparative Physiology A.

[34]  Heiner Römer,et al.  Representation of auditory distance within a central neuropil of the bushcricketMygalopsis marki , 2004, Journal of Comparative Physiology A.

[35]  A. Moiseff,et al.  Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior , 1983, Journal of comparative physiology.

[36]  A. Stumpner Picrotoxin eliminates frequency selectivity of an auditory interneuron in a bushcricket. , 1998, Journal of neurophysiology.

[37]  H. Römer,et al.  Organization of a sensory neuropile in the auditory pathway of two groups of orthoptera , 1988, The Journal of comparative neurology.

[38]  Reinhard Lakes-Harlan,et al.  Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera) , 2001, Journal of Comparative Physiology A.

[39]  H. Römer,et al.  Synaptic mechanisms of monaural and binaural processing in the locust , 1982 .

[40]  Barbara Schmitz,et al.  Phonotaxis inGryllus campestris L. (Orthoptera, Gryllidae) , 2004, Journal of comparative physiology.

[41]  Eliot A. Brenowitz,et al.  Species specificity and temperature dependency of temporal processing by the auditory midbrain of two species of treefrogs , 1985, Journal of Comparative Physiology A.

[42]  A. Stumpner,et al.  Comparison of morphology and physiology of two plurisegmental sound-activated interneurones in a bushcricket , 1999, Journal of Comparative Physiology A.

[43]  The physiology of ascending auditory interneurons in the tettigoniidCaedicia simplex (Orthoptera: Ensifera): response properties and a model of integration in the afferent auditory pathway , 1983, Journal of comparative physiology.

[44]  G. Pollack,et al.  Steering responses of flying crickets to sound and ultrasound: Mate attraction and predator avoidance. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[45]  J. Fullard,et al.  Information processing at a central synapse suggests a noise filter in the auditory pathway of the noctuid moth , 2004, Journal of Comparative Physiology A.

[46]  B. Lewis,et al.  Two-tone suppression and song coding by ascending neurones in the cricketGryllus campestris L. , 1984, Journal of Comparative Physiology A.

[47]  Central branchings of three sensory axons from a moth ear (Agrotis segetum, Noctuidae) , 1982 .

[48]  Heiner Römer,et al.  Die Informationsverarbeitung tympanaler Rezeptorelemente vonLocusta migratoria (Acrididae, Orthoptera) , 2004, Journal of comparative physiology.

[49]  G. Boyan Two-tone suppression of an identified auditory neurone in the brain of the cricketGryllus bimaculatus (De Geer) , 2004, Journal of comparative physiology.

[50]  R. M. Hennig,et al.  Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis , 1997, Journal of Comparative Physiology A.

[51]  J. Rheinlaender,et al.  Intracellular studies on auditory processing in the metathoracic ganglion of the locust , 1981, Journal of comparative physiology.

[52]  T. G. Forrest,et al.  Hearing in mole crickets (Orthoptera: Gryllotalpidae) at sonic and ultrasonic frequencies. , 1998, The Journal of experimental biology.

[53]  D. Helversen,et al.  Interaural intensity and time discrimination in an unrestraint grasshopper: a tentative behavioural approach , 1988, Journal of Comparative Physiology A.

[54]  P. Fonseca,et al.  Song discrimination by male cicadas Cicada barbara lusitanica (Homoptera, Cicadidae). , 2002, The Journal of experimental biology.

[55]  Synaptic inputs to the omega neuron of the cricket Teleogryllus oceanicus: differences in EPSP waveforms evoke by low and high sound frequencies , 2004, Journal of Comparative Physiology A.

[56]  D D Yager,et al.  Structure, development, and evolution of insect auditory systems , 1999, Microscopy research and technique.

[57]  Cynthia F. Moss,et al.  Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus , 1990, Journal of Comparative Physiology A.

[58]  G. Wendler,et al.  Pattern Recognition and Localization in Cricket Phonotaxis , 1990 .

[59]  J. P. Miller,et al.  Stimulus-response properties of cricket cereal filiform receptors , 1995, Journal of Comparative Physiology A.

[60]  Heiner Römer,et al.  Morphology and physiology of auditory interneurons in the metathoracic ganglion of the locust , 1984, Journal of Comparative Physiology A.

[61]  A. Stumpner A species-specific frequency filter through specific inhibition, not specific excitation , 2002, Journal of Comparative Physiology A.

[62]  G. Pollack,et al.  Selective attention in an insect auditory neuron , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  J. Rheinlaender Transmission of acoustic information at three neuronal levels in the auditory system ofDecticus verrucivorus (Tettigoniidae, Orthoptera) , 1975, Journal of comparative physiology.

[64]  Franz Huber,et al.  Frequency and temporal pattern-dependent phonotaxis of crickets (Teleogryllus oceanicus) during tethered flight and compensated walking , 2004, Journal of Comparative Physiology A.

[65]  Low-pass filtering of sound signals by a high-frequency brain neuron and its input in the cricketAcheta domestica L. , 1988, Journal of Comparative Physiology A.

[66]  Jörg Lewald,et al.  High-frequency sound transmission in natural habitats: implications for the evolution of insect acoustic communication , 1992, Behavioral Ecology and Sociobiology.

[67]  J. Schul Neuronal basis of phonotactic behaviour in Tettigonia viridissima : processing of behaviourally relevant signals by auditory afferents and thoracic interneurons , 1997, Journal of Comparative Physiology A.

[68]  G. Pollack,et al.  Age‐Dependent occurrence of an ascending axon on the omega neuron of the cricket, Teleogryllus oceanicus , 1986, The Journal of comparative neurology.

[69]  Matija Gogala,et al.  SONGS OF FOUR CICADA SPECIES FROM THAILAND , 1995 .

[70]  Tateo Shimozawa,et al.  Varieties of filiform hairs: range fractionation by sensory afferents and cereal interneurons of a cricket , 1984, Journal of Comparative Physiology A.

[71]  An interneurone of unusual morphology is tuned to the female song frequency in the bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). , 1999, The Journal of experimental biology.

[72]  Jürgen Rheinlaender,et al.  The precision of auditory lateralization in the cricket, Gryllus bimaculatus , 1982 .

[73]  A. Surlykke,et al.  Hearing of the Australian whistling moth, Hecatesia thyridion , 1989, Die Naturwissenschaften.

[74]  A. Selverston,et al.  Synaptic connectivity between cricket auditory interneurons as studied by selective photoinactivation , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[75]  J. Fullard,et al.  Interneurones responding to sound in the tobacco budworm mothHeliothis virescens (Noctuidae): morphological and physiological characteristics , 2004, Journal of Comparative Physiology A.

[76]  J. Hildebrand,et al.  Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. , 1997, Journal of neurophysiology.

[77]  Dagmar von Helversen,et al.  Acoustic pattern recognition in a grasshopper: processing in the time or frequency domain? , 1998, Biological Cybernetics.

[78]  B. Ronacher,et al.  Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.) , 2002, Journal of Comparative Physiology A.

[79]  Age-correlated changes and juvenile hormone III regulation of the syllable period specific responses of the L3 auditory interneurons in the cricket, Acheta domesticus , 1992, Journal of Comparative Physiology A.

[80]  Heiner Römer,et al.  Insect hearing in the field , 1986, Journal of Comparative Physiology A.

[81]  K. D. Roeder,et al.  Nerve Cells and Insect Behavior , 1998 .

[82]  A. Stumpner,et al.  Recognition of a two-element song in the grasshopper Chorthippus dorsatus (Orthoptera: Gomphocerinae) , 1992, Journal of Comparative Physiology A.

[83]  A Moiseff,et al.  Time and intensity cues are processed independently in the auditory system of the owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  Local interneurons mediating excitation and inhibition onto ascending neurons in the auditory pathway of grasshoppers , 2004, Naturwissenschaften.

[85]  Heiner Römer,et al.  Insect hearing in the field , 2004, Journal of Comparative Physiology A.

[86]  K. G. Hill,et al.  Functional development of the auditory system of the cricket,Teleogryllus commodus , 1978, Journal of comparative physiology.

[87]  Rohini Balakrishnan,et al.  Song pattern recognition in the grasshopper Chorthippus biguttulus: the mechanism of syllable onset and offset detection , 2001, Journal of Comparative Physiology A.

[88]  J. H. Casseday,et al.  The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  F. Huber,et al.  Sound localisation in crickets , 1994, Journal of Comparative Physiology A.

[90]  Axel Michelsen,et al.  Time Resolution in Auditory Systems , 1985, Proceedings in Life Sciences.

[91]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[92]  Franz Huber,et al.  Primary auditory neurons in crickets: Physiology and central projections , 1980, Journal of comparative physiology.

[93]  A. Watson,et al.  Distribution of synapses on two ascending interneurones carrying frequency‐specific information in the auditory system of the cricket: Evidence for gabaergic inputs , 1994, The Journal of comparative neurology.

[94]  J. Schul,et al.  Song recognition by temporal cues in a group of closely related bushcricket species (genus Tettigonia) , 1998, Journal of Comparative Physiology A.

[95]  N. Suga,et al.  Peripheral auditory tuning for fine frequency analysis by the CF-FM bat,Rhinolophus ferrumequinum , 2004, Journal of comparative physiology.

[96]  Heiner Römer,et al.  Insect hearing in the field , 2004, Journal of Comparative Physiology A.

[97]  J. H. Casseday,et al.  Timing in the auditory system of the bat. , 1999, Annual review of physiology.

[98]  D. Helversen,et al.  Species Recognition and Acoustic Localization in Acridid Grasshoppers: A Behavioral Approach , 1983 .

[99]  K. D. Roeder Brain interneurons in noctuoid moths: binaural excitation and slow potentials. , 1973, Journal of insect physiology.

[100]  H. Rehbein Auditory neurons in the ventral cord of the locust: Morphological and functional properties , 2004, Journal of comparative physiology.

[101]  L. Miller,et al.  Parallel processing of afferent input by identified interneurones in the auditory pathway of the noctuid moth Noctua pronuba (L.) , 2004, Journal of Comparative Physiology A.

[102]  D. von Helversen,et al.  Selective phonotaxis in Tettigonia cantans and T. viridissima in song recognition and discrimination , 1998, Journal of Comparative Physiology A.

[103]  Processing of calling songs by an L‐shaped neuron in the prothoracic ganglion of the female cricket, Acheta domesticus , 1988 .

[104]  L. Miller,et al.  Auditory input to motor neurons of the dorsal longitudinal flight muscles in a noctuid moth (Barathra brassicae L.) , 2004, Journal of Comparative Physiology A.

[105]  Christian K. Machens,et al.  Representation of Acoustic Communication Signals by Insect Auditory Receptor Neurons , 2001, The Journal of Neuroscience.

[106]  M Konishi,et al.  Effects of Interaural Intensity Difference on the Processing of Interaural Time Difference in the Owl’s Nucleus Laminaris , 1997, The Journal of Neuroscience.

[107]  Barbara Schmitz Phonotaxis inGryllus campestris L. (Orthoptera, Gryllidae) , 1985, Journal of Comparative Physiology A.

[108]  J. Rheinlaender,et al.  The directional sensitivity of a bush cricket ear: a behavioural and neurophysiological study of Leptophyes punctatissima , 1986 .

[109]  G. Pollack,et al.  Temporal Pattern as a Cue for Species-Specific Calling Song Recognition in Crickets , 1979, Science.

[110]  Projection areas and branching patterns of the tympanal receptor cells in migratory locusts, Locusta migratoria and Schistocerca gregaria , 1988, Cell and Tissue Research.

[111]  B. Ronacher,et al.  Auditory interneurones in the metathoracic ganglion of the grasshopper Chorthippus biguttulus. II: Processing of temporal patterns of the song of the male , 1991 .

[112]  K. Schildberger,et al.  Temporal selectivity of identified auditory neurons in the cricket brain , 2004, Journal of Comparative Physiology A.

[113]  Bernhard Ronacher,et al.  Routes and stations in the processing of auditory directional information in the CNS of a grasshopper, as revealed by surgical experiments , 1986, Journal of Comparative Physiology A.

[114]  G. Pollack,et al.  Who, what, where? recognition and localization of acoustic signals by insects , 2000, Current Opinion in Neurobiology.

[115]  Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus). , 2000, Journal of neurophysiology.

[116]  Brian Lewis,et al.  Peripheral auditory directionality in the cricketGryllus campestris L.,Teleogryllus oceanicus Le Guillou) , 1983, Journal of comparative physiology.

[117]  P. D. Manley,et al.  Peripheral Hearing Mechanisms in Reptiles and Birds , 1990, Zoophysiology.

[118]  Gerald S. Pollack,et al.  Discrimination of calling song models by the cricket,Teleogryllus oceanicus: the influence of sound direction on neural encoding of the stimulus temporal pattern and on phonotactic behavior , 1986, Journal of Comparative Physiology A.

[119]  B. Ronacher,et al.  Long rise times of sound pulses in grasshopper songs improve the directionality cues received by the CNS from the auditory receptors , 1993, Journal of Comparative Physiology A.

[120]  H. Römer,et al.  A gain-control mechanism for processing of chorus sounds in the afferent auditory pathway of the bushcricket Tettigonia viridissima (Orthoptera; Tettigoniidae) , 2000, Journal of Comparative Physiology A.

[121]  R. Hoy,et al.  Audition in the praying mantis,Mantis religiosa L.: identification of an interneuron mediating ultrasonic hearing , 1989, Journal of Comparative Physiology A.

[122]  Franz Huber,et al.  Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket,Gryllus campestris L. , 1982, Journal of comparative physiology.

[123]  G. Boyan Common synaptic drive to segmentally homologous interneurons in the locust , 1992, The Journal of comparative neurology.

[124]  Organization of the auditory pathway in the thoracic ganglia of noctuid moths , 1990, The Journal of comparative neurology.

[125]  W. Rössler,et al.  Auditory receptor organs in the forelegs of Gampsocleis gratiosa (Tettigoniidae): Morphology and function of the organs in comparison to the frequency parameters of the conspecific song , 1993 .

[126]  B. Schmitz,et al.  Morphological and physiological changes in central auditory neurons following unilateral foreleg amputation in larval crickets , 1986, Journal of Comparative Physiology A.

[127]  Analysis of the cricket auditory system by acoustic stimulation using a closed sound field , 1981, Journal of comparative physiology.

[128]  Lutz-Jörg Adam,et al.  Neurophysiologie des Hörens und Bioakustik einer Feldheuschrecke (Locusta migratoria) , 1969, Zeitschrift für vergleichende Physiologie.

[129]  M. Hörner,et al.  The function of auditory neurons in cricket phonotaxis , 2004, Journal of Comparative Physiology A.

[130]  D. Young,et al.  PHONOTAXIS IN THE CICADAS CYSTOSOMA SAUNDERSII AND CYCLOCHILA AUSTRALASIAE , 1997 .

[131]  Central projections of primary auditory fibres in Tettigoniidae (Orthoptera: Ensifera) , 1983, Journal of comparative physiology.

[132]  Physiology of auditory receptors in two species of Tettigoniidae (Orthoptera: Ensifera) , 1984, Journal of Comparative Physiology A.

[133]  D. Tank,et al.  In Vivo Ca2+ Dynamics in a Cricket Auditory Neuron: An Example of Chemical Computation , 1994, Science.

[134]  A. Stumpner,et al.  Tonotopic organization of auditory receptors of the bushcricket Pholidoptera griseoaptera (Tettigoniidae, Decticinae) , 1998, Cell and Tissue Research.

[135]  J. Fullard The Sensory Coevolution of Moths and Bats , 1998 .

[136]  D. von Helversen,et al.  Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing? , 1995, Journal of Comparative Physiology A.

[137]  Cell responses to acoustic stimuli in the pterothoracic ganglion of two noctuoid moths , 2004, Journal of Comparative Physiology A.

[138]  D. Helversen Parallel processing in auditory pattern recognition and directional analysis by the grasshopperChorthippus biguttulus L. (Acrididae) , 1984, Journal of Comparative Physiology A.

[139]  R. Wyttenbach,et al.  Categorical Perception of Sound Frequency by Crickets , 1996, Science.

[140]  B. Oldfield Tonotopic organisation of auditory receptors in tettigoniidae (Orthoptera: Ensifera) , 1982, Journal of comparative physiology.

[141]  F. Lang Noise filtering in the auditory system of Locusta migratoria L , 1996, Journal of Comparative Physiology.

[142]  Gerald Langner,et al.  Periodicity coding in the auditory system , 1992, Hearing Research.

[143]  J. Rheinlaender,et al.  Bilateral coding of sound direction in the CNS of the bushcricketTettigonia viridissima L. (Orthoptera, Tettigoniidae) , 1980, Journal of comparative physiology.

[144]  Hans Scharstein,et al.  Cricket phonotaxis: localization depends on recognition of the calling song pattern , 1989, Journal of Comparative Physiology A.

[145]  G. Pollack,et al.  Response properties of prothoracic, interganglionic, sound-activated interneurons in the cricketTeleogryllus oceanicus , 1987, Journal of Comparative Physiology A.

[146]  Bernhard Ronacher,et al.  Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron , 1988, Journal of Comparative Physiology A.

[147]  D. Oertel The role of timing in the brain stem auditory nuclei of vertebrates. , 1999, Annual review of physiology.

[148]  Bernhard Ronacher,et al.  Neurophysiological Aspects of Song Pattern Recognition and Sound Localization in Grasshoppers , 1994 .

[149]  A. Surlykke,et al.  Temporal coding in the auditory receptor of the moth ear , 1988, Journal of Comparative Physiology A.

[150]  Processing of unilateral and bilateral auditory inputs by the ON1 and L1 interneurons of the cricket Acheta domesticus and comparison to other cricket species , 1995, Journal of Comparative Physiology A.

[151]  D. Helversen,et al.  Recognition of sex in the acoustic communication of the grasshopper Chorthippus biguttulus (Orthoptera, Acrididae) , 1997, Journal of Comparative Physiology A.

[152]  K. Kalmring,et al.  The physiological characteristics of the primary sensory neurons of the complex tibial organ ofDecticus verrucivorus L. (Orthoptera, Tettigonioidae) , 1978, Journal of comparative physiology.

[153]  B. Ronacher,et al.  Temperature dependence of temporal resolution in an insect nervous system , 2002, Journal of Comparative Physiology A.

[154]  F. Theunissen,et al.  Extraction of Sensory Parameters from a Neural Map by Primary Sensory Interneurons , 2000, The Journal of Neuroscience.

[155]  H. Römer,et al.  Responses to model songs of auditory neurons in the thoracic ganglia and brain of the locust , 1985, Journal of Comparative Physiology A.

[156]  J. Rheinlaender,et al.  ‘Time–intensity trading’ in locust auditory interneurones , 1979, Nature.

[157]  R Krahe,et al.  Temporal integration vs. parallel processing: coping with the variability of neuronal messages in directional hearing of insects , 2000, The European journal of neuroscience.

[158]  Klaus Kalmring The afferent auditory pathway in the ventral cord ofLocusta migratoria (Acrididae) , 2005, Journal of comparative physiology.

[159]  A. Watson,et al.  Distribution of synapses on two local auditory interneurones, ON1 and ON2, in the prothoracic ganglion of the cricket: relationships with GABA-immunoreactive neurones , 1996, Cell and Tissue Research.

[160]  J. D. Crawford,et al.  Feature-detecting auditory neurons in the brain of a sound-producing fish , 1997, Journal of Comparative Physiology A.

[161]  D. Helversen,et al.  Evolution and function of auditory systems in insects , 2001, Naturwissenschaften.

[162]  Bernhard Ronacher,et al.  Spike synchronization of tympanic receptor fibres in a grasshopper (Chorthippus biguttulus L., Acrididae) , 1985, Journal of Comparative Physiology A.

[163]  Stumpner An auditory interneurone tuned to the male song frequency in the duetting bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae) , 1997, The Journal of experimental biology.

[164]  Morphology and physiology of local auditory interneurons in the prothoracic ganglion of the cricket Acheta domesticus , 1997 .