Modulation of auditory signal-to-noise ratios by efferent stimulation.

One of the primary challenges that sensory systems face is extracting relevant information from background noise. In the auditory system, the ear receives efferent feedback, which may help it extract signals from noise. Here we directly test the hypothesis that efferent activity increases the signal-to-noise ratio (SNR) of the ear, using the relatively simple teleost ear. Tone-evoked saccular potentials were recorded before and after efferent stimulation, and the SNR of the responses was calculated. In quiet conditions, efferent stimulation suppressed saccular responses to a tone, reducing the SNR. However, when masking noise was added, efferent stimulation increased the SNR of the saccular responses within a range of stimulus combinations. These data demonstrate that auditory efferent feedback can increase SNR in conditions where a signal is masked by noise, thereby enhancing the encoding of signals in noise. Efferent feedback thus performs a fundamental signal processing function, helping the animal to hear sounds in difficult listening conditions.

[1]  J. Guinan.  Physiology of Olivocochlear Efferents , 1996 .

[2]  Zhongmin Lu,et al.  Acoustic response properties of lagenar nerve fibers in the sleeper goby, Dormitator latifrons , 2003, Journal of Comparative Physiology A.

[3]  J. E. Frank,et al.  Mechanical Noise Enhances Signal Transmission in the Bullfrog Sacculus , 2003, Journal of the Association for Research in Otolaryngology.

[4]  P A Fuchs,et al.  Efferent regulation of hair cells in the turtle cochlea , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[5]  J. Fex.  Auditory activity in centrifugal and centripetal cochlear fibres in cat. A study of a feedback system. , 1962, Acta physiologica Scandinavica. Supplementum.

[6]  P. Nieder,et al.  Crossed olivocochlear bundle: electrical stimulation enhances masked neural responses to loud clicks. , 1970, Brain research.

[7]  S. Tomchik,et al.  Auditory physiology and anatomy of octavolateral efferent neurons in a teleost fish , 2005, Journal of Comparative Physiology A.

[8]  A. Nuttall,et al.  Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. , 1988, The Journal of the Acoustical Society of America.

[9]  A. Bass,et al.  Directionality and frequency tuning of primary saccular afferents of a vocal fish, the plainfin midshipman (Porichthys notatus) , 2002, Journal of Comparative Physiology A.

[10]  A. Bass,et al.  Vocal Pathways Modulate Efferent Neurons to the Inner Ear and Lateral Line , 2005, The Journal of Neuroscience.

[11]  G. L. Rasmussen.  The olivary peduncle and other fiber projections of the superior olivary complex , 1946, The Journal of comparative neurology.

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

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

[14]  R. Galamboš.  Suppression of auditory nerve activity by stimulation of efferent fibers to cochlea. , 1956, Journal of neurophysiology.

[15]  M. Sachs,et al.  Effect of electrical stimulation of the crossed olivocochlear bundle on auditory nerve response to tones in noise. , 1987, Journal of neurophysiology.

[16]  J. H. Dewson,et al.  sone relationships to stimulus discrimination in noise. , 1968, Journal of neurophysiology.

[17]  Hallowell Davis,et al.  The Electrical Phenomena of the Cochlea and the Auditory Nerve , 1935 .

[18]  J. Guinan,et al.  Effects of crossed-olivocochlear-bundle stimulation on cat auditory nerve fiber responses to tones. , 1983, The Journal of the Acoustical Society of America.

[19]  Z. Lu,et al.  Coding of acoustic particle motion by utricular fibers in the sleeper goby, Dormitator latifrons , 2004, Journal of Comparative Physiology A.

[20]  R. Klinke,et al.  Efferent activity in the goldfish vestibular nerve and its influence on afferent activity , 1980, Pflügers Archiv.

[21]  T. Furukawa.  Effects of efferent stimulation on the saccule of goldfish. , 1981, The Journal of physiology.

[22]  Peter M. Narins,et al.  Coding of signals in noise by amphibian auditory nerve fibers , 1987, Hearing Research.

[23]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

[24]  M. Lugli,et al.  Acoustic communication in two freshwater gobies: the relationship between ambient noise, hearing thresholds and sound spectrum , 2003, Journal of Comparative Physiology A.

[25]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[26]  I. Russell,et al.  The activity of lateral-line efferent neurones in stationary and swimming dogfish. , 1972, The Journal of experimental biology.

[27]  S. Highstein,et al.  Miniature EPSPs and Sensory Encoding in the Primary Afferents of the Vestibular Lagena of the Toadfish, Opsanus tau , 1999, Annals of the New York Academy of Sciences.

[28]  S. Highstein,et al.  Visually mediated inhibition of lateral line primary afferent activity by the octavolateralis efferent system during predation in the free-swimming toadfish, Opsanus tau , 2004, Experimental Brain Research.

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

[30]  R. Fay,et al.  Dendritic arbors and central projections of physiologically characterized auditory fibers from the saccule of the toadfish, Opsanus tau , 1999, The Journal of comparative neurology.

[31]  R. Fay,et al.  Behavioral detection of acoustic particle motion by a teleost fish (Astronotus ocellatus): sensitivity and directionality , 1996, Journal of Comparative Physiology A.

[32]  T Kawase,et al.  Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. , 1993, Journal of neurophysiology.

[33]  T. Furukawa,et al.  Neurophysiological studies on hearing in goldfish. , 1967, Journal of neurophysiology.

[34]  R. Boyle,et al.  Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  A. Flock,et al.  Transducing mechanisms in the lateral line canal organ receptors. , 1965, Cold Spring Harbor symposia on quantitative biology.

[36]  T Kawase,et al.  Antimasking effects of the olivocochlear reflex. I. Enhancement of compound action potentials to masked tones. , 1993, Journal of neurophysiology.

[37]  S. Tomchik,et al.  Octavolateral projections and organization in the medulla of a teleost fish, the sleeper goby (Dormitator latifrons) , 2005, The Journal of comparative neurology.

[38]  Robert Joseph Wolfson,et al.  Ultrastructure of the Vestibular Sense Organ , 1966 .