Variability of spike trains and the processing of temporal patterns of acoustic signals—problems, constraints, and solutions

Object recognition and classification by sensory pathways is rooted in spike trains provided by sensory neurons. Nervous systems had to evolve mechanisms to extract information about relevant object properties, and to separate these from spurious features. In this review, problems caused by spike train variability and counterstrategies are exemplified for the processing of acoustic signals in orthopteran insects. Due to size limitations of their nervous system we expect to find solutions that are stripped to the computational basics. A key feature of auditory systems is temporal resolution, which is likely limited by spike train variability. Basic strategies to reduce such variability are to integrate over time, or to average across several neurons. The first strategy is constrained by its possible interference with temporal resolution. Grasshoppers do not seem to explore temporal integration much, in spite of the repetitive structure of their songs, which invites for ‘multiple looks’ at the signal. The benefits of averaging across neurons depend on uncorrelated responses, a factor that may be crucial for the performance and evolution of small nervous systems. In spite of spike train variability the temporal information necessary for the recognition of conspecifics is preserved to a remarkable degree in the auditory pathway.

[1]  B. Hedwig,et al.  A cephalothoracic command system controls stridulation in the acridid grasshopper Omocestus viridulus L. , 1994, Journal of neurophysiology.

[2]  Axel Michelsen,et al.  Strategies for Acoustic Communication in Complex Environments , 1983 .

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

[4]  N. Viemeister,et al.  Temporal integration and multiple looks. , 1991, The Journal of the Acoustical Society of America.

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

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

[7]  Activation and modulation of auditory receptors inLocusta migratoria by respiratory movements , 1988, Journal of Comparative Physiology A.

[8]  N. Elsner,et al.  How respiration affects auditory sensitivity in the grasshopper Chorthippus biguttulus (L.) , 1995, Journal of Comparative Physiology A.

[9]  A. Stumpner,et al.  Physiological variability of auditory neurons in a grasshopper , 1989, The Science of Nature.

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

[11]  R. H. Wiley,et al.  Reverberations and Amplitude Fluctuations in the Propagation of Sound in a Forest: Implications for Animal Communication , 1980, The American Naturalist.

[12]  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 .

[13]  J. Miller,et al.  Effects of adaptation on neural coding by primary sensory interneurons in the cricket cercal system. , 1997, Journal of neurophysiology.

[14]  G S Pollack,et al.  Sensory habituation of auditory receptor neurons: implications for sound localization. , 2000, The Journal of experimental biology.

[15]  Heiner Römer,et al.  The Sensory Ecology of Acoustic Communication in Insects , 1998 .

[16]  F. Barth,et al.  Vibratory communication in spiders , 1993, Journal of Comparative Physiology A.

[17]  G. Rose,et al.  Auditory midbrain neurons that count , 2002, Nature Neuroscience.

[18]  F Gilbert,et al.  Directional hearing of a grasshopper in the field. , 2000, The Journal of experimental biology.

[19]  H. Kriegbaum Female choice in the grasshopper Chorthippus biguttulus , 1989, Naturwissenschaften.

[20]  Jack W. Bradbury,et al.  Principles of Animal Communication , 1998 .

[21]  O. Helversen,et al.  Verhaltensgenetische Untersuchungen am akustischen Kommunikationssystem der Feldheuschrecken (Orthoptera, Acrididae) , 2005, Journal of comparative physiology.

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

[23]  Bernhard Ronacher,et al.  Single auditory neurons rapidly discriminate conspecific communication signals , 2003, Nature Neuroscience.

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

[25]  Bernhard Ronacher,et al.  Coding of a sexually dimorphic song feature by auditory interneurons of grasshoppers: the role of leading inhibition , 2001, Journal of Comparative Physiology A.

[26]  Klaus Reinhold,et al.  Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus , 2003, Animal Behaviour.

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

[28]  R M Hennig,et al.  Processing of auditory information in insects , 2004, Microscopy research and technique.

[29]  D. Helversen ‘Absolute steepness’ of ramps as an essential cue for auditory pattern recognition by a grasshopper (Orthoptera; Acrididae; Chorthippus biguttulus L.) , 1993, Journal of Comparative Physiology A.

[30]  M. Brinkmann,et al.  Mechanoelectric transduction in nematocytes of a hydropolyp (Corynidae) , 2004, Journal of Comparative Physiology A.

[31]  Gary J. Rose,et al.  Integration and recovery processes contribute to the temporal selectivity of neurons in the midbrain of the northern leopard frog, Rana pipiens , 2000, Journal of Comparative Physiology A.

[32]  G. Klump,et al.  Temporal summation in the European starling (Sturnus vulgaris). , 1990 .

[33]  R. M. Hennig Acoustic feature extraction by cross-correlation in crickets? , 2003, Journal of Comparative Physiology A.

[34]  H. C. Bennet-Clark,et al.  Size and scale effects as constraints in insect sound communication , 1998 .

[35]  F. Barth,et al.  A Spider’s World: Senses and Behavior , 2001 .

[36]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.

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

[38]  Jakob Tougaard,et al.  Receiver operating characteristics and temporal integration in an insect auditory receptor cell , 1999 .

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

[40]  R. R. Capranica,et al.  Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters , 1984, Journal of Comparative Physiology A.

[41]  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.

[42]  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.

[43]  A. V. Popov,et al.  Neuroethology of Acoustic Communication , 1978 .

[44]  J. Benda Single Neuron Dynamics — Models Linking Theory and Experiment , 2002 .

[45]  W. R. Garner The Processing of Information and Structure , 1974 .

[46]  Eric J. Warrant,et al.  Arthropod eye design and the physical limits to spatial resolving power , 1993, Progress in Neurobiology.

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

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

[49]  N. Elsner Neuroethology of sound production in gomphocerine grasshoppers (orthoptera: acrididae) , 1975, Journal of comparative physiology.

[50]  Bernhard Ronacher,et al.  Discrimination of behaviorally relevant signals by auditory receptor neurons , 2001, Neurocomputing.

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

[52]  J. Tougaard,et al.  Detection of short pure-tone stimuli in the noctuid ear: what are temporal integration and integration time all about? , 1998, Journal of Comparative Physiology A.

[53]  Reinhard Lakes-Harlan,et al.  Tympanal receptor cells of Schistocerca gregaria: Correlation of soma positions and dendrite attachment sites, central projections and physiologies , 1999 .

[54]  Dagmar von Helversen Gesang des Männchens und Lautschema des Weibchens bei der FeldheuschreckeChorthippus biguttulus (Orthoptera, Acrididae) , 1972, Journal of comparative physiology.

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

[56]  E. Warrant Seeing better at night: life style, eye design and the optimum strategy of spatial and temporal summation , 1999, Vision Research.

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

[58]  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.

[59]  G. Klump,et al.  Gap detection in the European starling (Sturnus vulgaris) , 1991, Journal of Comparative Physiology A.

[60]  R. Full,et al.  Capacity for sustained terrestrial locomotion in an insect: Energetics, thermal dependence, and kinematics , 1990, Journal of Comparative Physiology B.

[61]  Heiner Römer,et al.  Ecological Constraints for Sound Communication: From Grasshoppers to Elephants , 2001 .

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

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

[64]  R. Butlin,et al.  Comparisons among Morphological Characters and between Localities in the Chorthippus parallelus Hybrid Zone (Orthoptera: Acrididae) , 1991 .

[65]  A. J. Hudspeth,et al.  How the ear's works work , 1989, Nature.

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

[67]  B. Ronacher,et al.  Effects of signal duration on the recognition of masked communication signals by the grasshopper Chorthippus biguttulus , 2000, Journal of Comparative Physiology A.

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

[69]  Anthony Arak,et al.  Choice of singing sites by male bushcrickets (Tettigonia viridissima) in relation to signal propagation , 1992, Behavioral Ecology and Sociobiology.

[70]  D. Blumstein Acoustic Communication in Insects and Anurans : Common Problems and Diverse Solutions , 2002 .

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

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

[73]  A. Stumpner,et al.  Morphological and physiological differences of the auditory system in three related bushcrickets (Orthoptera: Phaneropteridae, Poecilimon) , 1992 .

[74]  B. Ronacher,et al.  Influence of amplitude modulated noise on the recognition of communication signals in the grasshopper Chorthippus biguttulus , 2003, Journal of Comparative Physiology A.

[75]  Anne Treisman,et al.  Properties, Parts, and Objects , 1986 .

[76]  H. Gerhardt,et al.  Female mate choice in treefrogs: static and dynamic acoustic criteria , 1991, Animal Behaviour.

[77]  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.

[78]  K. Reinhold,et al.  Dissecting the repeatability of female choice in the grasshopper Chorthippus biguttulus , 2002, Animal Behaviour.

[79]  H. Gerhardt,et al.  Temperature Coupling in the Vocal Communication System of the Gray Tree Frog, Hyla versicolor , 1978, Science.

[80]  O. V. Helversen,et al.  Separate localization of sound recognizing and sound producing neural mechanisms in a grasshopper , 2004, Journal of Comparative Physiology A.

[81]  M. Shadlen,et al.  Limits to the temporal fidelity of cortical spike rate signals , 2002, Nature Neuroscience.

[82]  H. Wolf,et al.  ‘Switching-off’ of an auditory interneuron during stridulation in the acridid grasshopperChorthippus biguttulus L. , 1986, Journal of Comparative Physiology A.

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

[84]  Acoustic behaviour of both sexes of the speckled bush cricket Leptophyes punctatissima , 1976 .

[85]  B. Grothe,et al.  Temporal processing in sensory systems , 2000, Current Opinion in Neurobiology.

[86]  David M. Green,et al.  Temporal Factors in Psychoacoustics , 1985 .

[87]  R. D. Semlitsch,et al.  Call duration as an indicator of genetic quality in male gray tree frogs. , 1998, Science.

[88]  J. Doherty Temperature coupling and trade-off phenomena in the acoustic communication system of the cricket, Gryllus bimaculatus De Geer (Gryllidae) , 1985 .

[89]  G. Boyan Another look at insect audition: The tympanic receptors as an evolutionary specialization of the chordotonal system , 1993 .

[90]  Dagmar,et al.  Verhaltensgenetische Untersuchungen am akustischen Kommunikationssystem der Feldheuschrecken (Orthoptera, Acrididae) , 1975, Journal of comparative physiology.

[91]  E. de Boer,et al.  Auditory Time Constants: A Paradox? , 1985 .

[92]  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.

[93]  R. Robertson,et al.  Effects of temperature on properties of flight neurons in the locust , 1994, Journal of Comparative Physiology A.

[94]  D. Helversen,et al.  Calling behavior in bushcrickets of the genusPoecilimon with differing communication systems (Orthoptera: Tettigonioidea, Phaneropteridae) , 1993, Journal of Insect Behavior.

[95]  M. Zuk,et al.  Exploitation of Sexual Signals by Predators and Parasitoids , 1998, The Quarterly Review of Biology.

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

[97]  F. Barth,et al.  Vibratory communication in spiders , 1992, Journal of Comparative Physiology A.

[98]  R. Meldola Sexual Selection , 1871, Nature.

[99]  D. Helversen,et al.  Acoustic communication in phaneropterid bushcrickets: species-specific delay of female stridulatory response and matching male sensory time window , 2004, Behavioral Ecology and Sociobiology.

[100]  Axel Michelsen,et al.  Biophysics of Sound Localization in Insects , 1998 .

[101]  Peter G. Gillespie,et al.  Molecular basis of mechanosensory transduction , 2001, Nature.

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

[103]  Adrienne L. Fairhall,et al.  Efficiency and ambiguity in an adaptive neural code , 2001, Nature.

[104]  Berthold Hedwig,et al.  Corollary Discharge Inhibition of Ascending Auditory Neurons in the Stridulating Cricket , 2003, The Journal of Neuroscience.

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

[106]  Behavioral determination of frequency resolution in the ear of the cricket,Teleogryllus oceanicus , 1982, Journal of comparative physiology.

[107]  Michael D. Beecher,et al.  SPECTROGRAPHIC ANALYSIS OF ANIMAL VOCALIZATIONS: IMPLICATIONS OF THE “UNCERTAINTY PRINCIPLE” , 1988 .

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

[109]  Klaus-Gerhard Heller,et al.  Bushcricket song structure and predation by the acoustically orienting parasitoid fly Therobia leonidei (Diptera: Tachinidae: Ormiini) , 1998, Behavioral Ecology and Sociobiology.

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

[111]  R R Hoy,et al.  Temperature coupling in cricket acoustic communication , 1992, Journal of Comparative Physiology A.

[112]  N. Elsner Neuroethology of sound production in gomphocerine grasshoppers (Orthoptera: Acrididae) , 2004, Journal of comparative physiology.

[113]  Berthold Hedwig,et al.  A corollary discharge maintains auditory sensitivity during sound production , 2002, Nature.

[114]  Eliot A. Brenowitz,et al.  Neural correlates of temperature coupling in the vocal communication system of the gray treefrog (Hyla versicolor) , 1985, Brain Research.

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

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

[117]  H. Römer Ecological Constraints for the Evolution of Hearing and Sound Communication in Insects , 1992 .

[118]  Friederike Lang,et al.  ACOUSTIC COMMUNICATION DISTANCES OF A GOMPHOCERINE GRASSHOPPER , 2000 .

[119]  Gary J. Rose,et al.  Long-term temporal integration in the anuran auditory system , 1998, Nature Neuroscience.

[120]  Andreas V. M. Herz,et al.  A Universal Model for Spike-Frequency Adaptation , 2003, Neural Computation.

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

[122]  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.

[123]  K. Prestwich,et al.  The Energetics of Acoustic Signaling in Anurans and Insects , 1994 .

[124]  Mark C. W. van Rossum,et al.  A Novel Spike Distance , 2001, Neural Computation.

[125]  Gerald S. Pollack,et al.  Neural Processing of Acoustic Signals , 1998 .

[126]  G. Klump,et al.  Comodulation masking release in a songbird , 1995, Hearing Research.

[127]  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.

[128]  E. Ball,et al.  The grasshopper, Drosophila and neuronal homology (advantages of the insect nervous system for the neuroscientist) , 1993, Progress in Neurobiology.

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

[130]  Israel Nelken,et al.  Responses of auditory-cortex neurons to structural features of natural sounds , 1999, Nature.

[131]  B. Ronacher,et al.  Neuronal adaptation improves the recognition of temporal patterns in a grasshopper , 2004, Journal of Comparative Physiology A.

[132]  H. Römer,et al.  Strategies for hearing in noise: peripheral control over auditory sensitivity in the bushcricket sciarasaga quadrata (Austrosaginae: tettigoniidae) , 1998 .

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

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

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

[136]  Modulation of auditory responsiveness in stridulating grasshoppers , 1990, Journal of Comparative Physiology A.

[137]  R. Butlin,et al.  A hybrid zone between two subspecies of the grasshopper Chorthippus parallelus along the Pyrenees: the west end , 1994, Heredity.

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

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

[140]  H. Römer,et al.  Sensory basis for sound intensity discrimination in the bushcricket Requena verticalis (Tettigoniidae, Orthoptera) , 1998, Journal of Comparative Physiology A.

[141]  B. Ronacher,et al.  Song recognition in the grasshopper Chorthippus biguttulus is not impaired by shortening song signals: implications for neuronal encoding , 1998, Journal of Comparative Physiology A.

[142]  B. Hedwig,et al.  Singing and hearing: neuronal mechanisms of acoustic communication in Orthopterans , 2001 .