Central auditory neurophysiology of a sound-producing fish: the mesencephalon of Pollimyrus isidori (Mormyridae)

This paper describes the auditory neurophysiology of the mesencephalon of P. isidori, a soundproducing mormyrid fish. Mormyrids have a specialized pressure-sensitive auditory periphery, and anatomical studies indicate that acoustic information is relayed to the mesencephalic nucleus MD. Fish were stimulated with tone bursts and clicks, and responses of MD neurons were recorded extracellularly. Auditory neurons had best frequencies (BF) and best sensitivities (BS) that fell within the range of frequencies and levels of the natural communication sounds of these fish. BSs were in the range of 0 to — 35 dB (re. 1.0 dyne/cm2). Many of the neurons were tuned (Q10 dB: 2–6), and had BFs in the range of 100–300 Hz where the animal's sounds have their peak energy. A range of different physiological cell types were encountered, including phasic, sustained, and complex neurons. Some of the sustained neurons showed strong phase-locking to tones. Many neurons exhibited non-monotonic rate-level functions. Frequencies flanking the BF often caused a reduction in spontaneous activity suggesting inhibition. Many neurons showed excellent representation of click-trains, and some showed a temporal representation of inter-click-intervals with errors less than 1 ms.

[1]  A. Sutterlin,et al.  Visual-auditory unit responses in the goldfish tegmentum. , 1970, Journal of neurophysiology.

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

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

[4]  Ad. J. Kalmijn,et al.  Hydrodynamic and Acoustic Field Detection , 1988 .

[5]  F. Haugede-Carre The mormyrid mesencephalon. II. The medio-dorsal nucleus of the torus semicircularis: Afferent and efferent connections studied with the HRP method , 1983, Brain Research.

[6]  The Fourier transform of a peristimulus time histogram can lead to erroneous results , 1986, Brain Research.

[7]  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.

[8]  Binaural Interaction in the Cod , 1980 .

[9]  K. Frank,et al.  CHAPTER 2 – MICROELECTRODES FOR RECORDING AND STIMULATION , 1964 .

[10]  C. Bell Some Central Connections of Medullary Octavolateral Centers in a Mormyrid Fish , 1981 .

[11]  J. E. Rose,et al.  A metal-filled microelectrode. , 1953, Science.

[12]  Arthur N. Popper,et al.  Functional Aspects of the Evolution of the Auditory System of Actinopterygian Fish , 1992 .

[13]  Stephen M. Echteler,et al.  Organization of central auditory pathways in a teleost fish,Cyprinus carpio , 1985, Journal of Comparative Physiology A.

[14]  E D Young,et al.  Organization of dorsal cochlear nucleus type IV unit response maps and their relationship to activation by bandlimited noise. , 1991, Journal of neurophysiology.

[15]  J. Tautz,et al.  The EOD sound response in weakly electric fish , 1981, Journal of comparative physiology.

[16]  P. Morse Vibration and Sound , 1949, Nature.

[17]  G. Rose A temporal-processing mechanism for all species? , 1986, Brain, behavior and evolution.

[18]  A. Popper,et al.  Sound reception in two anabantid fishes. , 1987, Comparative biochemistry and physiology. A, Comparative physiology.

[19]  R. Fay Masking and suppression in auditory nerve fibers of the goldfish, Carassius auratus , 1991, Hearing Research.

[20]  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.

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

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

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

[24]  M. Hagedorn,et al.  Acoustic communication in an electric fish,Pollimyrus isidori (Mormyridae) , 1986, Journal of Comparative Physiology A.

[25]  J. Marshall,et al.  Sound Production by the Elephant-Nose Fish, Gnathonemus petersi (Pisces, Mormyridae) , 1973 .

[26]  Leonard Maler,et al.  Cytology and immunocytochemistry of the nucleus extrolateralis anterior of the mormyrid brain: possible role of GABAergic synapses in temporal analysis , 2004, Anatomy and Embryology.

[27]  P. S. Enger,et al.  Hearing in herring. , 1967, Comparative biochemistry and physiology.

[28]  J. D. Crawford Sex recognition by electric cues in a sound-producing mormyrid fish, pollimyrus isidori , 1991 .

[29]  A. Popper,et al.  Auditory sensitivity and psychophysical tuning curves in the elephant nose fish,Gnathonemus petersii , 1984, Journal of Comparative Physiology A.

[30]  Arthur N. Popper,et al.  Auditory response of saccular neurons of the catfish,Ictalurus punctatus , 1984, Journal of Comparative Physiology A.

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

[32]  C. A. Mccormick Evolution of Central Auditory Pathways in Anamniotes , 1992 .

[33]  Robert D Frisina,et al.  Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement , 1990, Hearing Research.

[34]  C. H. Page Electrophysiological study of auditory responses in the goldfish brain. , 1970, Journal of neurophysiology.

[35]  R. Fay,et al.  Adaptation effects on amplitude modulation detection: Behavioral and neurophysiological assessment in the goldfish auditory system , 1985, Hearing Research.

[36]  C. Bell Central distribution of octavolateral afferents and efferents in a teleost (mormyridae) , 1981, The Journal of comparative neurology.

[37]  W. Plassmann,et al.  Coding of amplitude-modulated tones in the central auditory system of catfish , 1985, Hearing Research.

[38]  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.

[39]  M. Sachs,et al.  Effects of nonlinearities on speech encoding in the auditory nerve. , 1979, The Journal of the Acoustical Society of America.

[40]  M. Sachs,et al.  Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. , 1989, Journal of neurophysiology.

[41]  T. Furukawa Synaptic interaction at the mauthner cell of goldfish. , 1966, Progress in brain research.

[42]  S. Echteler Tonotopic organization in the midbrain of a teleost fish , 1985, Brain Research.