Varying Overall Sound Intensity to the Two Ears Impacts Interaural Level Difference Discrimination Thresholds by Single Neurons in the Lateral Superior Olive

Abstract

The lateral superior olive (LSO) is one of the earliest sites in the auditory pathway involved in processing acoustical cues to sound location. LSO neurons encode the interaural level difference (ILD) cue to azimuthal location. Here we investigated the effect of variations in the overall stimulus levels of sounds at the two ears on the sensitivity of LSO neurons to small differences in ILDs of pure tones. The neuronal firing rate versus ILD functions were found to depend greatly on the overall stimulus level, typically shifting along the ILD axis toward the excitatory ear and attaining greater maximal firing rates as stimulus level increased. Seventy-five percent of neurons showed significant shifts with changes in overall sound level. The range of ILDs corresponding to best neural acuity for ILDs shifted accordingly. In a simulation using the empirical data, when the overall stimulus level was randomly changed from one trial to the next, the neural discrimination thresholds for ILD, or ILD acuities, were worsened by 50-60% across the population of neurons relative to fixed stimulus levels whether ILD acuity was measured at the azimuthal midline or the ILD pedestal producing the best acuity. The impairment in ILD discrimination was attributed to the increased neural response variance imparted by varying the stimulus level. These results contrast to those observed in psychophysical studies where ILD discrimination thresholds under similar experimental conditions are invariant to overall changes in stimulus level. A simple computational model that incorporated the antagonistic inputs of bilateral LSO nuclei as well as the dorsal nuclei of the lateral lemniscus to the inferior colliculus produced a more robust encoding of ILD even in the setting of roving stimulus level. Testable predictions of this model and comparison to other computational models addressing stimulus invariance were considered.

Sound frequency-invariant neural coding of a frequency-dependent cue to sound source location

“…Collectively, the half-maximal ILD, ILD dynamic range, and rate-ILD slope capture the attributes of a neuron's response that, together with spike variance, determine its capacity to encode ILD (Tollin et al 2008;Tsai et al 2010; see also Fig. 3).…”

“…To facilitate analysis over a broad range of continuously varying ILDs, the fitted sigmoid function relating spike count to ILD (see above) was used to compute y=(ILD) for each neuron. Then, the ILD-dependent variance [(ILD) 2 ] for each neuron was approximated by fitting a two-parameter power function of the form y ϭ ax b , where x is spike count and a and b are free parameters (Tsai et al 2010). Across the ILD-sensitive neurons (n ϭ 103), the variance vs. spike count data were well described by the power function (mean R 2 ϭ 0.89 Ϯ 0.1).…”

“…While ILD coding by neurons in the LSO is highly dependent on overall sound level, neurons in the ICC have been shown to be more robust (invariant in their response) to changes in sound level (see Tsai et al 2010 for review). Since we did not manipulate overall sound level in these experiments, we cannot speculate how our results would change across a range of overall levels.…”

“…Since we did not manipulate overall sound level in these experiments, we cannot speculate how our results would change across a range of overall levels. However, based on prior studies we would expect ILD coding to persist in many ICC neurons across a range of sound levels (see Tsai et al 2010).…”

Localization of Click Trains and Speech by Cats: the Negative Level Effect

“…It has also been shown that neurons in the auditory cortex are level tolerant when encoding horizontal and vertical sound locations (Zhou and Wang 2012). Other physiological studies have demonstrated that certain neurons in the inferior colliculus and the auditory cortex maintain their spatial sensitivity at high sound levels (Irvine and Gago 1990;Miller and Recanzone 2009), whereas the sensitivity of neurons in the lateral superior olive decreases with sound level (Tsai et al 2010), although these studies only examined sound localization in azimuth.…”