Peripheral encoding of behaviorally relevant acoustic signals in a vocal fish: single tones

Abstract The midshipman fish, Porichthys notatus, generates acoustic signals for intraspecific communication. Nesting males produce long-duration “hums” which attract gravid females and can be effectively mimicked by pure tones. In this study we examine the encoding of tonal signals by the midshipman peripheral auditory system. Single-unit recordings were made from afferents innervating the sacculus while presenting sounds via an underwater loudspeaker. Units were characterized by iso-intensity spike rate and vector strength of synchronization curves, as well as by peri-stimulus time histograms. Additionally, response-intensity curves and responses to long-duration (up to 10 s) stimuli were obtained. As has been seen in other teleosts, afferents had highly variable activity profiles. Excitatory frequencies ranged from 60 to over 300 Hz with most units responding best around 70 or 140 Hz. Thresholds at 90 Hz ranged from 95 to 145 dB re 1 μPa. Strong synchronization provided a robust temporal code of frequency, comparable to that described for goldfish. Spike rate showed varying degrees of adaptation but high rates were generally maintained even for 10-s stimuli. The midshipman peripheral auditory system is well suited to encoding conspecific communication signals, but nonetheless shares many response patterns with the auditory system of other teleosts.

[1]  J. Steen,et al.  The sensitivity of the cod sacculus to directional and non-directional sound stimuli , 1979 .

[2]  G. Cailliet,et al.  The mating call of the plainfin midshipman fish, Porichthys notatus , 1983 .

[3]  R. Fay,et al.  Source level discrimination by the lateral line system of the mottled sculpin, Cottus bairdi. , 1993, The Journal of the Acoustical Society of America.

[4]  Mismatch between Sound Production and Hearing in the Oyster Toadfish , 1981 .

[5]  J. Fish,et al.  Hearing thresholds from toadfish, Opsanus tau, measured in the laboratory and field. , 1972, The Journal of the Acoustical Society of America.

[6]  R. Fay,et al.  Acoustic response and tuning in saccular nerve fibers of the goldfish (Carassius auratus). , 1986, The Journal of the Acoustical Society of America.

[7]  R. Fay,et al.  Directional response properties of saccular afferents of the toadfish, Opsanus tau , 1997, Hearing Research.

[8]  R. Baker,et al.  Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. , 1985, Journal of neurophysiology.

[9]  R. Fay,et al.  Sound detection and processing by fish: critical review and major research questions. , 1993, Brain, behavior and evolution.

[10]  R. Fay Auditory frequency discrimination in the goldfish (Carassius auratus). , 1970 .

[11]  R. Fay Suppression and excitation in auditory nerve fibers of the goldfish,Carassius auratus , 1990, Hearing Research.

[12]  R. Fay Coding of Acoustic Information in the Eighth Nerve , 1981 .

[13]  K. Frisch The Sense of Hearing in Fish , 1938, Nature.

[14]  R. Fay Sound intensity processing by the goldfish. , 1985, Journal of the Acoustical Society of America.

[15]  R. Fay,et al.  The effects of temperature change and transient hypoxia on auditory nerve fiber response in the goldfish (Carassius auratus) , 1992, Hearing Research.

[16]  A. Popper,et al.  Hair cell orientation patterns on the saccules of juvenile and adult toadfish, Opsanus tau. , 1995, Acta zoologica.

[17]  Richard R. Fay,et al.  Frequency Selectivity, Adaptation, and Suppression in Goldfish Auditory Nerve Fibers , 1986 .

[18]  O. Sand,et al.  Field studies of hearing in two species of flatfish Pleuronectes platessa (L.) and limanda limanda (L.) (family pleuronectidae). , 1974, Comparative biochemistry and physiology. A, Comparative physiology.

[19]  A. Popper,et al.  Encoding of acoustic directional information by saccular afferents of the sleeper goby, Dormitator latifrons , 1998, Journal of Comparative Physiology A.

[20]  Richard R. Fay,et al.  Structure and Function in Teleost Auditory Systems , 1978 .

[21]  P. Fraser,et al.  Frequency Characteristics of Primary Auditory Neurons from the Ear of the Cod, Gadus morhua L. , 1981 .

[22]  R. Fay,et al.  Diversity in frequency response properties of saccular afferents of the toadfish, Opsanus tau , 1997, Hearing Research.

[23]  Richard R. Fay,et al.  Sound Detection and Processing by Fish: Critical Review and Major Research Questions (Part 1 of 2) , 1993 .

[24]  J. Pickles An Introduction to the Physiology of Hearing , 1982 .

[25]  R. Fay,et al.  Hearing in Vertebrates: A Psychophysics Databook , 1988 .

[26]  Andrew H. Bass,et al.  Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish , 2010 .

[27]  Sheryl Coombs,et al.  The Morphology and Evolution of the Ear in Actinopterygian Fishes , 1982 .

[28]  D. Bodnar,et al.  Complementary explana-tions for existing phenotypes in an acoustic communication system , 1999 .

[29]  Christopher Platt,et al.  Fine Structure and Function of the Ear , 1981 .

[30]  R. Fay,et al.  Response dynamics of goldfish saccular fibers: effects of stimulus frequency and intensity on fibers with different tuning, sensitivity, and spontaneous activity. , 1987, Journal of the Acoustical Society of America.

[31]  A R Palmer,et al.  Intensity coding in low-frequency auditory-nerve fibers of the guinea pig. , 1991, The Journal of the Acoustical Society of America.

[32]  A. L. Megela Diversity of adaptation patterns in responses of eighth nerve fibers in the bullfrog, Rana catesbeiana. , 1984, The Journal of the Acoustical Society of America.

[33]  Anthony D. Hawkins,et al.  The Hearing Abilities of Fish , 1981 .

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

[35]  R. Fay,et al.  Neurophysiological Mechanisms of Intensity Discrimination in the Goldfish , 1981 .

[36]  M. Cohen,et al.  Electrophysiological observations on hearing and sound production in the fish, Porichthys notatus. , 1967, The Journal of experimental zoology.

[37]  G. K. Yates,et al.  Dynamic effects in the input/output relationship of auditory nerve , 1987, Hearing Research.

[38]  R. Fay The goldfish ear codes the axis of acoustic particle motion in three dimensions. , 1984, Science.

[39]  A H Bass,et al.  Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. , 1998, The Journal of the Acoustical Society of America.

[40]  J. Goldberg,et al.  Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. , 1969, Journal of neurophysiology.

[41]  E. Batschelet Circular statistics in biology , 1981 .

[42]  日本音響学会,et al.  Comparative Studies of Hearing in Vertebrates , 1980, Proceedings in Life Sciences.

[43]  R. Fay Coding of information in single auditory-nerve fibers of the goldfish. , 1978, The Journal of the Acoustical Society of America.