An auditory feature detection circuit for sound pattern recognition

Brain neurons form auditory feature detector circuit for song pattern recognition in acoustically communicating crickets. From human language to birdsong and the chirps of insects, acoustic communication is based on amplitude and frequency modulation of sound signals. Whereas frequency processing starts at the level of the hearing organs, temporal features of the sound amplitude such as rhythms or pulse rates require processing by central auditory neurons. Besides several theoretical concepts, brain circuits that detect temporal features of a sound signal are poorly understood. We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song. The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide. This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.

[1]  R R Hoy,et al.  Hybrid cricket auditory behavior: evidence for genetic coupling in animal communication. , 1977, Science.

[2]  R. Hoy Acoustic communication in crickets: a model system for the study of feature detection. , 1978, Federation proceedings.

[3]  B. Hedwig,et al.  Pattern recognition in field crickets: concepts and neural evidence , 2014, Journal of Comparative Physiology A.

[4]  J. Doherty,et al.  Hybrid Tree Frogs: Vocalizations of Males and Selective Phonotaxis of Females , 1983, Science.

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

[6]  G. Langner,et al.  Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Merionesunguiculatus ): two different coding strategies for pitch and rhythm? , 1997, Journal of Comparative Physiology A.

[7]  G. Rose,et al.  Interval-counting neurons in the anuran auditory midbrain: factors underlying diversity of interval tuning , 2010, Journal of Comparative Physiology A.

[8]  Hoy Rr,et al.  Acoustic communication in crickets: a model system for the study of feature detection. , 1978 .

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

[10]  Catherine E. Carr,et al.  Processing of Temporal Information in the Brain , 1993 .

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

[12]  M. Vater,et al.  Neural maps for target range in the auditory cortex of echolocating bats , 2014, Current Opinion in Neurobiology.

[13]  Jan Clemens,et al.  Computational principles underlying recognition of acoustic signals in grasshoppers and crickets , 2014, Journal of Comparative Physiology A.

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

[15]  Holger G. Krapp,et al.  Multiplication and stimulus invariance in a looming-sensitive neuron , 2004, Journal of Physiology-Paris.

[16]  J. Leo van Hemmen,et al.  Neuronal identification of acoustic signal periodicity , 2007, Biological Cybernetics.

[17]  K. Hildebrandt,et al.  Neural maps in insect versus vertebrate auditory systems , 2014, Current Opinion in Neurobiology.

[18]  B. Hedwig,et al.  Corollary discharge inhibition of wind-sensitive cercal giant interneurons in the singing field cricket , 2014, Journal of neurophysiology.

[19]  Masakazu Konishi,et al.  Robustness of Multiplicative Processes in Auditory Spatial Tuning , 2004, The Journal of Neuroscience.

[20]  S. Hooper,et al.  A computational role for slow conductances: single-neuron models that measure duration , 2002, Nature Neuroscience.

[21]  G. Pollack Analysis of temporal patterns of communication signals , 2001, Current Opinion in Neurobiology.

[22]  Benedikt Grothe,et al.  Hyperpolarization-activated current (Ih) in the inferior colliculus: distribution and contribution to temporal processing. , 2003, Journal of neurophysiology.

[23]  B. Hedwig,et al.  Cellular basis for singing motor pattern generation in the field cricket (Gryllus bimaculatus DeGeer) , 2012, Brain and behavior.

[24]  H Bullock Theodore,et al.  The Problem of Recognition in an Analyzer Made of Neurons , 2012 .

[25]  M. Konishi,et al.  Axonal delay lines for time measurement in the owl's brainstem. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[26]  B Hedwig,et al.  Processing of species-specific auditory patterns in the cricket brain by ascending, local, and descending neurons during standing and walking. , 2011, Journal of neurophysiology.

[27]  W Reichardt,et al.  Functional structure of a mechanism of perception of optical movement , 1958 .

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

[29]  Jakob Christensen-Dalsgaard,et al.  Temporally selective processing of communication signals by auditory midbrain neurons. , 2011, Journal of neurophysiology.

[30]  Masakazu Konishi,et al.  Deciphering the Brain's Codes , 1999, Neural Computation.

[31]  Jan Clemens,et al.  Time and timing in the acoustic recognition system of crickets , 2014, Front. Physiol..

[32]  I. Nelken,et al.  Single neuron and population coding of natural sounds in auditory cortex , 2014, Current Opinion in Neurobiology.

[33]  B. Hedwig,et al.  NEUROLAB, a comprehensive program for the analysis of neurophysiological and behavioural data , 1992, Journal of Neuroscience Methods.

[34]  Matthias H Hennig,et al.  The Sound of Silence: Ionic Mechanisms Encoding Sound Termination , 2011, Neuron.

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

[36]  Franz Huber,et al.  Auditory behavior of the cricket , 2004, Journal of comparative physiology.

[37]  Dean V. Buonomano,et al.  Timing as an intrinsic property of neural networks: evidence from in vivo and in vitro experiments , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  A. Bass,et al.  Neural mechanisms and behaviors for acoustic communication in teleost fish , 2003, Progress in Neurobiology.

[39]  D. Buonomano,et al.  The neural basis of temporal processing. , 2004, Annual review of neuroscience.

[40]  A. Magnusson,et al.  Sound Rhythms Are Encoded by Postinhibitory Rebound Spiking in the Superior Paraolivary Nucleus , 2011, The Journal of Neuroscience.

[41]  Alexander Borst,et al.  In search of the holy grail of fly motion vision , 2014, The European journal of neuroscience.

[42]  K. Shaw,et al.  Genomic linkage of male song and female acoustic preference QTL underlying a rapid species radiation , 2009, Proceedings of the National Academy of Sciences.

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

[44]  L A JEFFRESS,et al.  A place theory of sound localization. , 1948, Journal of comparative and physiological psychology.

[45]  B Hedwig,et al.  Mechanisms underlying phonotactic steering in the cricket Gryllus bimaculatus revealed with a fast trackball system , 2005, Journal of Experimental Biology.