From microseconds to seconds and minutes—time computation in insect hearing

The computation of time in the auditory system of insects is of relevance at rather different time scales, covering a large range from microseconds to several minutes. At the one end of this range, only a few microseconds of interaural time differences are available for directional hearing, due to the small distance between the ears, usually considered too small to be processed reliably by simple nervous systems. Synapses of interneurons in the afferent auditory pathway are, however, very sensitive to a time difference of only 1–2 ms provided by the latency shift of afferent activity with changing sound direction. At a much larger time scale of several tens of milliseconds to seconds, time processing is important in the context species recognition, but also for those insects where males produce acoustic signals within choruses, and the temporal relationship between song elements strongly deviates from a random distribution. In these situations, some species exhibit a more or less strict phase relationship of song elements, based on phase response properties of their song oscillator. Here we review evidence on how this may influence mate choice decisions. In the same dimension of some tens of milliseconds we find species of katydids with a duetting communication scheme, where one sex only performs phonotaxis to the other sex if the acoustic response falls within a very short time window after its own call. Such time windows show some features unique to insects, and although its neuronal implementation is unknown so far, the similarity with time processing for target range detection in bat echolocation will be discussed. Finally, the time scale being processed must be extended into the range of many minutes, since some acoustic insects produce singing bouts lasting quite long, and female preferences may be based on total signaling time.

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

[2]  H. Gerhardt,et al.  A precedence effect underlies preferences for calls with leading pulses in the grey treefrog, Hyla versicolor , 2010, Animal Behaviour.

[3]  N Suga,et al.  Biosonar and neural computation in bats. , 1990, Scientific American.

[4]  Lars Chittka,et al.  Speed-accuracy tradeoffs in animal decision making. , 2009, Trends in ecology & evolution.

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

[6]  J. Rheinlaender,et al.  Cues for male phonotaxis in the duetting bushcricketLeptophyes punctatissima , 1989, Journal of Comparative Physiology A.

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

[8]  R. D. Alexander,et al.  EVOLUTIONARY CHANGE IN CRICKET ACOUSTICAL COMMUNICATION , 1962 .

[9]  H. Römer,et al.  Fast and reliable decisions for a dynamic song parameter in field crickets , 2010, Journal of Comparative Physiology A.

[10]  Manfred Hartbauer,et al.  Mechanisms for synchrony and alternation in song interactions of the bushcricket Mecopoda elongata (Tettigoniidae: Orthoptera) , 2005, Journal of Comparative Physiology A.

[11]  Michael D Greenfield,et al.  Psychoacoustics of female phonotaxis and the evolution of male signal interactions in Orthoptera , 1995 .

[12]  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.

[13]  K. Reinhold Variation of Acoustic Courtship Signals in Insects and Amphibians: No Evidence for Bimodality, but Identical Dependence on Duration , 2009 .

[14]  H. Römer,et al.  Evolutionary transition from stretch to hearing organs in ancient grasshoppers , 1998, Nature.

[15]  Peter M. Narins,et al.  Chorus dynamics of a neotropical amphibian assemblage: comparison of computer simulation and natural behaviour , 1989, Animal Behaviour.

[16]  Michael D Greenfield,et al.  Females prefer leading males: relative call timing and sexual selection in katydid choruses , 1998, Animal Behaviour.

[17]  M. K. Tourtellot,et al.  Precedence effects and the evolution of chorusing , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  Michael D Greenfield,et al.  The complex auditory scene at leks: balancing antipredator behaviour and competitive signalling in an acoustic moth , 2011, Animal Behaviour.

[19]  D. J. Robinson,et al.  Female response song in the ephippigerines Steropleurus stali and Platystolus obvius (Orthoptera, Tettigoniidae) , 1974 .

[20]  H S Colburn,et al.  The precedence effect. , 1999, The Journal of the Acoustical Society of America.

[21]  M. Ryan,et al.  THE SENSORY BASIS OF SEXUAL SELECTION FOR COMPLEX CALLS IN THE TÚNGARA FROG, PHYSALAEMUS PUSTULOSUS (SEXUAL SELECTION FOR SENSORY EXPLOITATION) , 1990, Evolution; international journal of organic evolution.

[22]  W. Bailey,et al.  The Tettigoniidae: biology, systematics and evolution. , 1990 .

[23]  Axel Michelsen,et al.  Tuned directionality in cricket ears , 1995, Nature.

[24]  H. Römer,et al.  Sound transmission and directional hearing in field crickets: neurophysiological studies outdoors , 2010, Journal of Comparative Physiology A.

[25]  R. Gibson,et al.  How do animals choose their mates? , 1996, Trends in ecology & evolution.

[26]  G. Pollack Sensory cues for sound localization in the cricket Teleogryllus oceanicus: interaural difference in response strength versus interaural latency difference , 2003, Journal of Comparative Physiology A.

[27]  R. Fay Acoustic Communication , 2003, Springer Handbook of Auditory Research.

[28]  R. Hoy,et al.  The midline metathoracic ear of the praying mantis, Mantis religiosa , 1987, Cell and Tissue Research.

[29]  Jan Clemens,et al.  Computational principles underlying the recognition of acoustic signals in insects , 2013, Journal of Computational Neuroscience.

[30]  H. Kokko The Lekking Game: Can Female Choice Explain Aggregated Male Displays? , 1997 .

[31]  J. Schul,et al.  Selective phonotaxis in Neoconocephalus nebrascensis (Orthoptera: Tettigoniidae): call recognition at two temporal scales , 2008, Journal of Comparative Physiology A.

[32]  G. Pollack,et al.  Neural representation of sound amplitude by functionally different auditory receptors in crickets. , 2001, The Journal of the Acoustical Society of America.

[33]  Norman Lee,et al.  A precedence effect resolves phantom sound source illusions in the parasitoid fly Ormia ochracea , 2009, Proceedings of the National Academy of Sciences.

[34]  Frank E. Hanson,et al.  Control of flashing in fireflies , 1981, Journal of comparative physiology.

[35]  C E Carr,et al.  Processing of temporal information in the brain. , 1993, Annual review of neuroscience.

[36]  Michael J Beran,et al.  Chimpanzees (Pan troglodytes) respond to nonvisible sets after one-by-one addition and removal of items. , 2004, Journal of comparative psychology.

[37]  Neville Passmore,et al.  Synchronized courtship in fiddler crabs , 1998, Nature.

[38]  Johanna Mappes,et al.  Adaptive significance of synchronous chorusing in an acoustically signalling wolf spider , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  Daniel Robert,et al.  Directional hearing in insects , 2005 .

[40]  A. Meixner,et al.  Acoustic and Associated Behavior of the Coneheaded Katydid, Neoconocephalus nebrascensis (Orthoptera: Tettigoniidae) , 1986 .

[41]  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.

[42]  Michael J. Ryan,et al.  The role of synchronized calling, ambient light, and ambient noise, in anti-bat-predator behavior of a treefrog , 1982, Behavioral Ecology and Sociobiology.

[43]  A. V. Popov,et al.  Physics of directional hearing in the cricket Gryllus bimaculatus , 1994, Journal of Comparative Physiology A.

[44]  M. Ryan,et al.  Directional Patterns of Female Mate Choice and the Role of Sensory Biases , 1992, The American Naturalist.

[45]  T. J. Walker,et al.  Acoustic Synchrony: Two Mechanisms in the Snowy Tree Cricket , 1969, Science.

[46]  R A Wyttenbach,et al.  Demonstration of the precedence effect in an insect. , 1993, The Journal of the Acoustical Society of America.

[47]  J. Schwartz THE FUNCTION OF CALL ALTERNATION IN ANURAN AMPHIBIANS: A TEST OF THREE HYPOTHESES , 1987, Evolution; international journal of organic evolution.

[48]  Michael D Greenfield,et al.  Cooperation and Conflict in the Evolution of Signal Interactions , 1994 .

[49]  G. Höbel Interaction between signal timing and signal feature preferences: causes and implications for sexual selection , 2010, Animal Behaviour.

[50]  M. Kirkpatrick,et al.  The evolution of mating preferences and the paradox of the lek , 1991, Nature.

[51]  Neuronal correlates of a preference for leading signals in the synchronizing bushcricket Mecopoda elongata (Orthoptera, Tettigoniidae) , 2011, Journal of Experimental Biology.

[52]  M. Petrie,et al.  VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES , 1997, Biological reviews of the Cambridge Philosophical Society.

[53]  Anthony Arak,et al.  Orthopteran Mating Systems: Sexual Competition in a Diverse Group of Insects, Darryl T. Gwynne, Glenn K. Morris (Eds.). Westview Press, Boulder, Colorado (1983), xvii , 1984 .

[54]  M. Ryan,et al.  Sexual selection for sensory exploitation in the frog Physalaemus pustulosus , 1990, Nature.

[55]  K. C. Shaw,et al.  Forum: Role of Weight and Acoustic Parameters, Including Nature of Chorusing, in the Mating Success of Males of the Katydid, Amblycorypha Parvipennis (Orthoptera: Tettigoniidae) , 1991 .

[56]  Ronald R. Hoy,et al.  Physiology of the Auditory Afferents in an Acoustic Parasitoid Fly , 2002, The Journal of Neuroscience.

[57]  Barbara Webb,et al.  Robots in invertebrate neuroscience , 2002, Nature.

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

[59]  Jan Clemens,et al.  Feature Extraction and Integration Underlying Perceptual Decision Making during Courtship Behavior , 2013, The Journal of Neuroscience.

[60]  N. Suga,et al.  Encoding of target range and its representation in the auditory cortex of the mustached bat , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[62]  Peter M. Narins,et al.  Characterization of the advertisement call oscillator in the frogEleutherodactylus coqui , 1985, Journal of Comparative Physiology A.

[63]  H. Römer,et al.  Chirp rate is independent of male condition in a synchronising bushcricket. , 2006, Journal of insect physiology.

[64]  B. Hedwig,et al.  Calling Song Recognition in Female Crickets: Temporal Tuning of Identified Brain Neurons Matches Behavior , 2012, The Journal of Neuroscience.

[65]  D. Otte Evolution of Cricket Songs , 1992 .

[66]  Jan W. H. Schnupp,et al.  On hearing with more than one ear: lessons from evolution , 2009, Nature Neuroscience.

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

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

[69]  R. Miles,et al.  Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea. , 1995, The Journal of the Acoustical Society of America.

[70]  B. Truax Acoustic Communication , 1985 .

[71]  A. Moiseff,et al.  Firefly Synchrony: A Behavioral Strategy to Minimize Visual Clutter , 2010, Science.

[72]  O. V. Helversen,et al.  Song pattern recognition and an auditory time window in the female bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae) , 1994, Journal of Comparative Physiology A.

[73]  R. Hoy,et al.  Hawaiian courtship songs: evolutionary innovation in communication signals of Drosophila. , 1988, Science.

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

[75]  Michael D Greenfield Evolution of Acoustic Communication in the Genus Neoconocephalus: Discontinuous Songs, Synchrony, and Interspecific Interactions , 1990 .

[76]  Michael D Greenfield,et al.  DUET SINGING AND FEMALE CHOICE IN THE BUSHCRICKET PHANEROPTERA NANA , 2001 .

[77]  Sexual Selection and Sensory Exploitation , 1999 .

[78]  J. Schwartz,et al.  Male calling behavior, female discrimination and acoustic interference in the Neotropical treefrog Hyla microcephala under realistic acoustic conditions , 1993, Behavioral Ecology and Sociobiology.

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

[80]  Andrew C. Mason,et al.  Hyperacute directional hearing in a microscale auditory system , 2001, Nature.

[81]  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.

[82]  R. Balakrishnan,et al.  Synchrony during acoustic interactions in the bushcricket Mecopoda ‘Chirper’ (Tettigoniidae:Orthoptera) is generated by a combination of chirp-by-chirp resetting and change in intrinsic chirp rate , 2006, Journal of Comparative Physiology A.

[83]  J. Stradner,et al.  Selective attention in a synchronising bushcricket: physiology, behaviour and ecology , 2007, Journal of Comparative Physiology A.

[84]  G. K. Morris,et al.  Orthopteran mating systems : sexual competition in a diverse group of insects , 1983 .

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

[86]  N. Suga,et al.  Cortical neurons sensitive to combinations of information-bearing elements of biosonar signals in the mustache bat. , 1978, Science.

[87]  J L Cranford,et al.  Localization of paired sound sources in cats: effects of variable arrival times. , 1982, The Journal of the Acoustical Society of America.

[88]  M. Kavanagh THE EFFICIENCY OF SOUND PRODUCTION IN TWO CRICKET SPECIES, GRYLLOTALPA AUSTRALIS AND TELEOGRYLLUS COMMODUS (ORTHOPTERA: GRYLLOIDEA) , 1987 .

[89]  Michael D Greenfield,et al.  Mechanisms and evolution of synchronous chorusing: emergent properties and adaptive functions in Neoconocephalus katydids (Orthoptera: Tettigoniidae). , 2008, Journal of comparative psychology.

[90]  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.

[91]  R. Miles,et al.  Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea , 2004, Journal of Comparative Physiology A.

[92]  W. Bailey Insect duets: underlying mechanisms and their evolution , 2003 .

[93]  H. Gerhardt,et al.  Sources of Selection on Signal Timing in a Tree Frog , 2007 .

[94]  E. Sismondo,et al.  Synchronous, Alternating, and Phase-Locked Stridulation by a Tropical Katydid , 1990, Science.

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

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

[97]  J. Stradner,et al.  Neuroethology of female preference in the synchronously singing bushcricket Mecopoda elongata (Tettigoniidae; Orthoptera): why do followers call at all? , 2007, Journal of Experimental Biology.

[98]  J. Buck,et al.  Mechanism of Rhythmic Synchronous Flashing of Fireflies , 1968, Science.

[99]  Edward W. Large,et al.  Auditory Temporal Computation: Interval Selectivity Based on Post-Inhibitory Rebound , 2002, Journal of Computational Neuroscience.

[100]  Michael D Greenfield,et al.  Bat predation and the evolution of leks in acoustic moths , 2011, Behavioral Ecology and Sociobiology.

[101]  B. Hedwig,et al.  Contralateral inhibition as a sensory bias: the neural basis for a female preference in a synchronously calling bushcricket, Mecopoda elongata , 2002, The European journal of neuroscience.

[102]  Georg M. Klump,et al.  Mechanisms and Function of Call-Timing in Male-Male Interactions in Frogs , 1992 .

[103]  Berthold Hedwig,et al.  Pulses, patterns and paths: neurobiology of acoustic behaviour in crickets , 2006, Journal of Comparative Physiology A.

[104]  Franz Huber,et al.  Acoustic Communication in Insects and Anurans: Common Problems and Diverse Solutions , 2002 .

[105]  Michael D Greenfield,et al.  Katydid synchronous chorusing is an evolutionarily stable outcome of female choice , 1993, Nature.

[106]  H. Gaskell The precedence effect , 1983, Hearing Research.

[107]  M. Ryan Sexual selection, sensory systems and sensory exploitation. , 1990 .

[108]  H. Römer,et al.  Acoustic signal perception in a noisy habitat: lessons from synchronising insects , 2012, Journal of Comparative Physiology A.

[109]  T. U. Grafe,et al.  The function of call alternation in the African reed frog (Hyperolius marmoratus): precise call timing prevents auditory masking , 1996, Behavioral Ecology and Sociobiology.

[110]  Michael D Greenfield Signalers and Receivers: Mechanisms and Evolution of Arthropod Communication , 2002 .

[111]  M. Ryan,et al.  Sexual selection and signal evolution : the ghost of biases past , 1993 .

[112]  Richard D. Alexander,et al.  NATURAL SELECTION AND SPECIALIZED CHORUSING BEHAVIOR IN ACOUSTICAL INSECTS , 1975 .

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

[114]  J. Rheinlaender,et al.  Temporal parameters of male—female sound communication in Leptophyes punctatissima , 1986 .

[115]  Micheal L Dent,et al.  The precedence effect in three species of birds (Melopsittacus undulatus, Serinus canaria, and Taeniopygia guttata). , 2004, Journal of comparative psychology.

[116]  R. H. Wiley Lekking in Birds and Mammals: Behavioral and Evolutionary Issues , 1991 .

[117]  D. Lack,et al.  Ecological adaptations for breeding in birds , 1969 .

[118]  Michael D Greenfield,et al.  Synchronous and Alternating Choruses in Insects and Anurans: Common Mechanisms and Diverse Functions , 1994 .

[119]  B. Grothe,et al.  New roles for synaptic inhibition in sound localization , 2003, Nature Reviews Neuroscience.