Responses of neurons in the inferior colliculus of the rat to interaural time and intensity differences in transient stimuli: Implications for the latency hypothesis

Although the sensitivity to interaural intensity differences (IIDs) of neurons receiving excitatory - inhibitory binaural input (EI neurons) has been examined in numerous studies, the mechanisms underlying this sensitivity remain unclear. According to the 'latency hypotheses' neuronal sensitivity to IIDs reflects sensitivity to differences in the timing of ipsilateral and contralateral inputs that are produced as a consequence of the effects of intensity upon latency. If the latency hypothesis is correct, a neuron's responses over any given IID range should be predicted by its responses to the interaural time differences (ITDs) that are 'equivalent' to the IIDs tested, in the sense that they produce the same changes in the relative timing of inputs. This prediction from the latency hypotheses were examined by determining the sensitivity of EI neurons in the inferior colliculus of anesthetized rats to IIDs and ITDs in click stimuli, under conditions that allowed 'equivalent' ITDs to be estimated. In approximately 10% of the 41 neurons tested, the IID-sensitivity function was a perfect or near-perfect match to the equivalent-ITD function, indicating that IID sensitivity could be entirely accounted for in terms of sensitivity to intensity-produced neural time differences, as asserted by the latency hypothesis. For the majority of neurons, however, sensitivity to equivalent ITDs accounted only partially for the characteristics of the IID-sensitivity function; other features of the function in these cases appeared to reflect the operation of an additional factor, most probably the relative magnitude of the inputs from the two ears. Although the conclusions are qualified by the fact that one of the assumptions on which the estimation of equivalent ITDs was based was probably not satisfied for some neurons, the results suggest that intensity-produced changes in both the magnitude and the timing of excitatory and inhibitory inputs shape the IID sensitivity of most EI neurons.

[1]  J L HALL,et al.  Binaural interaction in the accessory superior olivary nucleus of the cat - an electrophysiological study of single neurons , 1963, The Journal of the Acoustical Society of America.

[2]  J. Kelly,et al.  Effects of superior olivary complex lesions on binaural responses in rat auditory cortex , 1993, Brain Research.

[3]  B M Clopton,et al.  Neural responses in the inferior colliculus of albino rat to binaural stimuli. , 1975, The Journal of the Acoustical Society of America.

[4]  S. Erulkar,et al.  SYNAPTIC MECHANISMS OF EXCITATION AND INHIBITION IN THE CENTRAL AUDITORY PATHWAY. , 1963, Journal of neurophysiology.

[5]  D. Caspary,et al.  On the role of GABA as an inhibitory neurotransmitter in inferior colliculus neurons: iontophoretic studies , 1989, Brain Research.

[6]  J. Boudreau,et al.  Cat superior olive S-segment cell discharge to tonal stimulation. , 1970, Contributions to Sensory Physiology.

[7]  M. Merchán,et al.  Intrinsic and commissural connections of the rat inferior colliculus , 1992, The Journal of comparative neurology.

[8]  M. Semple,et al.  Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences. , 1993, Journal of neurophysiology.

[9]  J. Kelly,et al.  Organization of auditory cortex in the albino rat: binaural response properties. , 1988, Journal of neurophysiology.

[10]  Dexter R. F. Irvine,et al.  The Auditory Brainstem: A Review of the Structure and Function of Auditory Brainstem Processing Mechanisms , 1986 .

[11]  G. Moushegian,et al.  Phase locking in monaural and binaural medullary neurons: implications for binaural phenomena. , 1978, The Journal of the Acoustical Society of America.

[12]  G. Pollak,et al.  GABA shapes sensitivity to interaural intensity disparities in the mustache bat's inferior colliculus: implications for encoding sound location , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  D. Sanes An in vitro analysis of sound localization mechanisms in the gerbil lateral superior olive , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Alexander Joseph Book reviewDischarge patterns of single fibers in the cat's auditory nerve: Nelson Yuan-Sheng Kiang, with the assistance of Takeshi Watanabe, Eleanor C. Thomas and Louise F. Clark: Research Monograph no. 35. Cambridge, Mass., The M.I.T. Press, 1965 , 1967 .

[15]  Pascal Barone,et al.  Physiology of Thalamus and Cortex , 1992 .

[16]  W. Melssen,et al.  Sensitivity for interaural time and intensity difference of auditory midbrain neurons in the grassfrog , 1990, Hearing Research.

[17]  G D Pollak,et al.  GABA shapes a topographic organization of response latency in the mustache bat's inferior colliculus , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  D. Anderson,et al.  Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation. , 1970, Journal of neurophysiology.

[19]  R E Kettner,et al.  Topography of binaural organization in primary auditory cortex of the cat: effects of changing interaural intensity. , 1986, Journal of neurophysiology.

[20]  J. Kelly,et al.  Binaural responses in rat inferior colliculus following kainic acid lesions of the superior olive: Interaural intensity difference functions , 1992, Hearing Research.

[21]  C. Faingold,et al.  Stimulation or blockade of the dorsal nucleus of the lateral lemniscus alters binaural and tonic inhibition in contralateral inferior colliculus neurons , 1993, Hearing Research.

[22]  L. Li,et al.  Inhibitory influence of the dorsal nucleus of the lateral lemniscus on binaural responses in the rat's inferior colliculus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  J. Kelly,et al.  Binaural interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice. , 1992, Journal of neurophysiology.

[24]  T. Yin,et al.  Interaural time sensitivity in medial superior olive of cat. , 1990, Journal of neurophysiology.

[25]  J. A. Hirsch,et al.  Responses of neurons in the cat's superior colliculus to acoustic stimuli. II. A model of interaural intensity sensitivity. , 1985, Journal of neurophysiology.

[26]  E Covey,et al.  Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat. , 1993, Journal of neurophysiology.

[27]  S Kuwada,et al.  Binaural interaction in low-frequency neurons in inferior colliculus of the cat. IV. Comparison of monaural and binaural response properties. , 1984, Journal of neurophysiology.

[28]  J. Kelly,et al.  Effects of superior olivary comples lesions on binaural responses in rat inferior colliculus , 1992, Brain Research.

[29]  G. Pollak,et al.  Binaural processing in the dorsal nucleus of the lateral lemniscus , 1994, Hearing Research.

[30]  J. E. Hind,et al.  Interaural time differences: implications regarding the neurophysiology of sound localization. , 1980, The Journal of the Acoustical Society of America.

[31]  Peter J. Moss,et al.  Binaural Interaction Models and Mechanisms , 1981 .

[32]  J M Harrison,et al.  Intensity changes at the ear as a function of the azimuth of a tone source: a comparative study. , 1970, The Journal of the Acoustical Society of America.

[33]  P D Coleman,et al.  Responses of single cells in cat inferior colliculus to binaural click stimuli: combinations of intensity levels, time differences and intensity differences. , 1970, Brain research.

[34]  J. Goldberg,et al.  Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. , 1968, Journal of neurophysiology.

[35]  Bruce H. Deatherage,et al.  Auditory Localization of Clicks , 1959 .

[36]  D. P. Phillips,et al.  Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural intensity differences , 1981, Hearing Research.

[37]  T C Yin,et al.  Responses of neurons in the cat's superior colliculus to acoustic stimuli. I. Monaural and binaural response properties. , 1985, Journal of neurophysiology.

[38]  E R Hafter,et al.  The combination of interaural time and intensity in the lateralization of high-frequency complex signals. , 1990, The Journal of the Acoustical Society of America.

[39]  D. R. F. Irvine,et al.  Interaural intensity difference sensitivity based on facilitatory binaural interaction in cat superior colliculus , 1984, Hearing Research.

[40]  M N Semple,et al.  Binaural processing of sound pressure level in the inferior colliculus. , 1987, Journal of neurophysiology.

[41]  R. Rajan,et al.  Normative N1 audiogram data for the barbiturate-anaesthetised domestic cat , 1991, Hearing Research.

[42]  D. Irvine,et al.  Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. I: Effects of variation of stimulus parameters , 1992, Hearing Research.

[43]  D. P. Phillips,et al.  Coding of interaural time differences of transients in auditory cortex of Rattus norvegicus: Implications for the evolution of mammalian sound localization , 1991, Hearing Research.

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

[45]  D. Caspary,et al.  Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons , 1991, Hearing Research.

[46]  J. Kelly,et al.  Kainic acid lesions of the dorsal nucleus of the lateral lemniscus: effects on binaural evoked responses in rat auditory cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  L. Kitzes,et al.  Patterns of responses of cortical cells to binaural stimulation , 1980, The Journal of comparative neurology.

[48]  D. Irvine Physiology of the Auditory Brainstem , 1992 .

[49]  G. Pollak Time is traded for intensity in the bat's auditory system , 1988, Hearing Research.

[50]  L. Carney,et al.  Responses of low-frequency cells in the inferior colliculus to interaural time differences of clicks: excitatory and inhibitory components. , 1989, Journal of neurophysiology.

[51]  T. Blackstad,et al.  The central nucleus of the inferior colliculus in rat: A Golgi and computer reconstruction study of neuronal and laminar structure , 1993, The Journal of comparative neurology.

[52]  R. Schmidt,et al.  Progress in Sensory Physiology , 1991, Progress in Sensory Physiology.

[53]  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.

[54]  D. Irvine,et al.  Binaural interaction in high-frequency neurons in inferior colliculus of the cat: effects of variations in sound pressure level on sensitivity to interaural intensity differences. , 1990, Journal of neurophysiology.