Neural Delays Shape Selectivity to Interaural Intensity Differences in the Lateral Superior Olive

Neurons in the lateral superior olive (LSO) respond selectively to interaural intensity differences (IIDs), one of the chief cues used to localize sounds in space. LSO cells are innervated in a characteristic pattern: they receive an excitatory input from the ipsilateral ear and an inhibitory input from the contralateral ear. Consistent with this pattern, LSO cells generally are excited by sounds that are more intense at the ipsilateral ear and inhibited by sounds that are more intense at the contralateral ear. Despite their relatively homogeneous pattern of innervation, IID selectivity varies substantially from cell to cell, such that selectivities are distributed over the range of IIDs that would be encountered in nature. For some time, researchers have speculated that the relative timing of the excitatory and inhibitory inputs to an LSO cell might shape IID selectivity. To test this hypothesis, we recorded from 50 LSO cells in the free-tailed bat while presenting stimuli that varied in interaural intensity and in interaural time of arrival. The results suggest that, for more than half of the cells, the latency of inhibition was several hundred microseconds longer than the latency of excitation. Increasing the intensity to the inhibitory ear shortened the latency of inhibition and brought the timing of the inputs from the two ears into register. Thus, a neural delay of the inhibition helped to define the IID selectivity of these cells, accounting for a significant part of the variation in selectivity among LSO cells.

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

[2]  N. Kiang,et al.  Stimulus coding in the auditory nerve and cochlear nucleus. , 1965 .

[3]  J. Boudreau,et al.  Binaural interaction in the cat superior olive S segment. , 1967, Journal of neurophysiology.

[4]  S. Erulkar Comparative aspects of spatial localization of sound. , 1972, Physiological reviews.

[5]  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.

[6]  G. Neuweiler,et al.  Interaural time and intensity coding in superior olivary complex and inferior colliculus of the echolocating bat Molossus ater. , 1985, Journal of neurophysiology.

[7]  Dexter R. F. Irvine,et al.  Auditory Brainstem Processing: Integration and Conclusions , 1986 .

[8]  Susanne Radtke-Schuller,et al.  A stereotaxic method for small animals using experimentally determined reference profiles , 1986, Journal of Neuroscience Methods.

[9]  E. Rubel,et al.  The ontogeny of inhibition and excitation in the gerbil lateral superior olive , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[11]  C Tsuchitani,et al.  The inhibition of cat lateral superior olive unit excitatory responses to binaural tone bursts. II. The sustained discharges. , 1988, Journal of neurophysiology.

[12]  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.

[13]  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.

[14]  M. Reed,et al.  A model for the computation and encoding of azimuthal information by the lateral superior olive. , 1990, The Journal of the Acoustical Society of America.

[15]  D. Caspary,et al.  Low-frequency neurons in the lateral superior olive exhibit phase-sensitive binaural inhibition. , 1991, Journal of neurophysiology.

[16]  E Covey,et al.  Binaural properties of single units in the superior olivary complex of the mustached bat. , 1991, Journal of neurophysiology.

[17]  J J Blum,et al.  Further studies of a model for azimuthal encoding: lateral superior olive neuron response curves and developmental processes. , 1991, The Journal of the Acoustical Society of America.

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

[19]  D. Irvine,et al.  Responses of neurons in the inferior colliculus of the rat to interaural time and intensity differences in transient stimuli: Implications for the latency hypothesis , 1995, Hearing Research.

[20]  T. Yin,et al.  Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. , 1995, Journal of neurophysiology.