Sensitivity to Interaural Temporal Disparities of Low- and High-Frequency Neurons in the Superior Olivary Complex. I. Heterogeneity of Responses

Abstract

Batra, Ranjan, Shigeyuki Kuwada, and Douglas C. Fitzpatrick. Sensitivity to interaural temporal disparities of low- and high-frequency neurons in the superior olivary complex. I. Heterogeneity of responses. J. Neurophysiol. 78: 1222–1236, 1997. Interaural temporal disparities (ITDs) are a cue for localization of sounds along the azimuth. Listeners can detect ITDs in the fine structure of low-frequency sounds and also in the envelopes of high-frequency sounds. Sensitivity to ITDs originates in the main nuclei of the superior olivary complex (SOC), the medial and lateral superior olives (MSO and LSO, respectively). This sensitivity is believed to arise from bilateral excitation converging on neurons of the MSO and ipsilateral excitation converging with contralateral inhibition on neurons of the LSO. Here we investigate whether the sensitivity of neurons in the SOC to ITDs can be adequately explained by one of these two mechanisms. Single and multiple units ( n = 124) were studied extracellularly in the SOC of unanesthetized rabbits. We found units that were sensitive to ITDs in the fine structure of low-frequency (<2 kHz) tones and also units that were sensitive to ITDs in the envelopes of sinusoidally amplitude-modulated high-frequency tones. For both categories there were “peak-type” units that discharged maximally at a particular ITD across frequencies or modulation frequencies. These units were consistent with an MSO-type mechanism. There were also “trough-type” units that discharged minimally at a particular ITD. These units were consistent with an LSO-type mechanism. There was a general trend for peak-type units to be located in the vicinity of the MSO and for trough-type units to be located in the vicinity of the LSO. Units of both types appeared to encode ITDs within the estimated free-field range of the rabbit (±300 μs). Many units had varying degrees of irregularities in their responses, which manifested themselves in one of two ways. First, for some units there was no ITD at which the response was consistently maximal or minimal across frequencies. Instead there was an ITD at which the unit consistently responded at some intermediate level. Second, a unit could display considerable jitter from frequency to frequency in the ITD at which it responded maximally or minimally. Units with irregular responses had properties that were continuous with those of other units. They therefore appeared to be variants of peak- and trough-type units. The irregular responses could be modeled by assuming additional phase-locked inputs to a neuron in the MSO or LSO. The function of irregularities may be to shift the ITD sensitivity of a neuron without requiring changes in the anatomic delays of its inputs.