Solutions to the Cocktail Party Problem in Insects: Selective Filters, Spatial Release from Masking and Gain Control in Tropical Crickets

Background Insects often communicate by sound in mixed species choruses; like humans and many vertebrates in crowded social environments they thus have to solve cocktail-party-like problems in order to ensure successful communication with conspecifics. This is even more a problem in species-rich environments like tropical rainforests, where background noise levels of up to 60 dB SPL have been measured. Principal Findings Using neurophysiological methods we investigated the effect of natural background noise (masker) on signal detection thresholds in two tropical cricket species Paroecanthus podagrosus and Diatrypa sp., both in the laboratory and outdoors. We identified three ‘bottom-up’ mechanisms which contribute to an excellent neuronal representation of conspecific signals despite the masking background. First, the sharply tuned frequency selectivity of the receiver reduces the amount of masking energy around the species-specific calling song frequency. Laboratory experiments yielded an average signal-to-noise ratio (SNR) of −8 dB, when masker and signal were broadcast from the same side. Secondly, displacing the masker by 180° from the signal improved SNRs by further 6 to 9 dB, a phenomenon known as spatial release from masking. Surprisingly, experiments carried out directly in the nocturnal rainforest yielded SNRs of about −23 dB compared with those in the laboratory with the same masker, where SNRs reached only −14.5 and −16 dB in both species. Finally, a neuronal gain control mechanism enhances the contrast between the responses to signals and the masker, by inhibition of neuronal activity in interstimulus intervals. Conclusions Thus, conventional speaker playbacks in the lab apparently do not properly reconstruct the masking noise situation in a spatially realistic manner, since under real world conditions multiple sound sources are spatially distributed in space. Our results also indicate that without knowledge of the receiver properties and the spatial release mechanisms the detrimental effect of noise may be strongly overestimated.

[1]  Yoshitaka Nakajima,et al.  Auditory Scene Analysis: The Perceptual Organization of Sound Albert S. Bregman , 1992 .

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

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

[4]  M. A. Bee,et al.  Sound source segregation in grey treefrogs: spatial release from masking by the sound of a chorus , 2007, Animal Behaviour.

[5]  Michael D Greenfield,et al.  Interspecific acoustic interactions among katydids Neoconocephalus: inhibition-induced shifts in diel periodicity , 1988, Animal Behaviour.

[6]  A S Feng,et al.  Detection of auditory signals by frog inferior collicular neurons in the presence of spatially separated noise. , 1998, Journal of neurophysiology.

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

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

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

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

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

[12]  Robert R. Capranica The untuning of the tuning curve: is it time? , 1992 .

[13]  Stewart H. Hulse,et al.  Auditory scene analysis in animal communication , 2002 .

[14]  H. Slabbekoorn,et al.  Cities Change the Songs of Birds , 2006, Current Biology.

[15]  P. Slater,et al.  Ambient noise, motor fatigue, and serial redundancy in chaffinch song , 2006, Behavioral Ecology and Sociobiology.

[16]  A. Basbaum,et al.  The senses : a comprehensive reference , 2008 .

[17]  E. C. Cherry Some Experiments on the Recognition of Speech, with One and with Two Ears , 1953 .

[18]  G. Pollack,et al.  3.31 – Invertebrate Auditory Pathways , 2008 .

[19]  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.

[20]  Ronald R. Hoy,et al.  Comparative Hearing: Insects , 1998, Springer Handbook of Auditory Research.

[21]  Eliot A. Brenowitz,et al.  The Role of Body Size, Phylogeny, and Ambient Noise in the Evolution of Bird Song , 1985, The American Naturalist.

[22]  Ruth Y Litovsky,et al.  The benefit of binaural hearing in a cocktail party: effect of location and type of interferer. , 2004, The Journal of the Acoustical Society of America.

[23]  R L Freyman,et al.  Spatial release from informational masking in speech recognition. , 2001, The Journal of the Acoustical Society of America.

[24]  H. Brumm,et al.  Acoustic Communication in Noise , 2005 .

[25]  Albert S. Feng,et al.  Free-field unmasking response characteristics of frog auditory nerve fibers: comparison with the responses of midbrain auditory neurons , 2001, Journal of Comparative Physiology A.

[26]  Daniel J. Mennill,et al.  A review of acoustic playback techniques for studying avian vocal duets , 2010 .

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

[28]  Mark E. Laidre,et al.  Principles of Animal Communication Principles of Animal Communication, 2nd edn. By JACK W. Bradbury & Sandra L. Vehrencamp. Sunderland, Massachusetts: Sinauer (2011). Pp. xiv + 697. Price $99.95. , 2012, Animal Behaviour.

[29]  R. Balakrishnan,et al.  Vertical stratification in an acoustically communicating ensiferan assemblage of a tropical evergreen forest in southern India , 2007, Journal of Tropical Ecology.

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

[31]  Romer Strategies for hearing in noise: peripheral control over auditory sensitivity in the bushcricket sciarasaga quadrata (Austrosaginae: tettigoniidae) , 1998, The Journal of experimental biology.

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

[33]  G. Klump,et al.  Auditory sensitivity in the great tit: perception of signals in the presence and absence of noise , 1998, Animal Behaviour.

[34]  Thierry Aubin,et al.  How do king penguins (Aptenodytes patagonicus apply the mathematical theory of information to communicate in windy conditions? , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  M. A. Bee,et al.  The cocktail party problem: what is it? How can it be solved? And why should animal behaviorists study it? , 2008, Journal of comparative psychology.

[36]  D. Kroodsma,et al.  Ecology and evolution of acoustic communication in birds , 1997 .

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

[38]  H. Brumm The impact of environmental noise on song amplitude in a territorial bird , 2004 .

[39]  Mark A. Bee,et al.  Finding a mate at a cocktail party: spatial release from masking improves acoustic mate recognition in grey treefrogs , 2008, Animal Behaviour.

[40]  W. Hödl,et al.  MASKING INTERFERENCE AND THE EVOLUTION OF THE ACOUSTIC COMMUNICATION SYSTEM IN THE AMAZONIAN DENDROBATID FROG ALLOBATES FEMORALIS , 2006, Evolution; international journal of organic evolution.

[41]  Manfred Hartbauer,et al.  Animal Communication Networks: Predation and noise in communication networks of neotropical katydids , 2005 .

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

[43]  U. Candolin The use of multiple cues in mate choice , 2003, Biological reviews of the Cambridge Philosophical Society.

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

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

[46]  B Hedwig,et al.  Neurite‐specific Ca2+ dynamics underlying sound processing in an auditory interneurone , 2007, Developmental neurobiology.

[47]  P. K. McGregor,et al.  Animal Communication Networks: Behaviours specific to communication networks , 2005 .

[48]  Michael J. Ryan,et al.  How cricket frog females deal with a noisy world: habitat-related differences in auditory tuning , 2005 .

[49]  W. Yost Auditory image perception and analysis: The basis for hearing , 1991, Hearing Research.

[50]  H. Slabbekoorn,et al.  Fluid dynamics: Vortex rings in a constant electric field , 2003, Nature.

[51]  D. Todt,et al.  Acoustic communication in noise: regulation of call characteristics in a New World monkey , 2004, Journal of Experimental Biology.

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

[53]  D. Thiele,et al.  The function of sound in male spacing behaviour in bush-crickets (Tettigoniidae, Orthoptera). , 1980 .

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

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

[56]  R. Dooling,et al.  Free-field binaural unmasking in budgerigars (Melopsittacus undulatus). , 1997, Behavioral neuroscience.

[57]  Manfred Hartbauer,et al.  Matched Filters, Mate Choice and the Evolution of Sexually Selected Traits , 2008, PloS one.

[58]  J. Sueur Cicada acoustic communication: potential sound partitioning in a multispecies community from Mexico (Hemiptera: Cicadomorpha: Cicadidae) , 2002 .

[59]  Lawrence M. Potash A signal detection problem and possible solution in Japanese quail (Coturnix coturnix japonica) , 1972 .

[60]  T. G. Forrest,et al.  SEXUAL SELECTION AND FEMALE CHOICE IN MOLE CRICKETS (SCAPTERISCUS: GRYLLOTALPIDAE): MODELLING THE EFFECTS OF INTENSITY AND MALE SPACING , 1991 .

[61]  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.

[62]  G. Horseman,et al.  Sound localisation in crickets , 2004, Journal of Comparative Physiology A.

[63]  R. Balakrishnan,et al.  THE ASSEMBLAGE OF ACOUSTICALLY COMMUNICATING CRICKETS OF A TROPICAL EVERGREEN FOREST IN SOUTHERN INDIA: CALL DIVERSITY AND DIEL CALLING PATTERNS , 2007 .

[64]  Alejandro A. Ríos-Chelén,et al.  Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird , 2011, Biology Letters.

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

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

[67]  W. Duellman,et al.  Acoustic Resource Partitioning in Anuran Communities , 1983 .

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

[69]  E. C. Cmm,et al.  on the Recognition of Speech, with , 2008 .

[70]  Klaus Riede,et al.  High background noise shapes selective auditory filters in a tropical cricket , 2011, Journal of Experimental Biology.

[71]  W. Hödl,et al.  HABITAT ACOUSTICS OF A NEOTROPICAL LOWLAND RAINFOREST , 2003 .