Effect of instantaneous frequency glides on interaural time difference processing by auditory coincidence detectors

Abstract

Detecting interaural time difference (ITD) is crucial for sound localization. The temporal accuracy required to detect ITD, and how ITD is initially encoded, continue to puzzle scientists. A fundamental question is whether the monaural inputs to the binaural ITD detectors differ only in their timing, when temporal and spectral tunings are largely inseparable in the auditory pathway. Here, we investigate the spectrotemporal selectivity of the monaural inputs to ITD detector neurons of the owl. We found that these inputs are selective for instantaneous frequency glides. Modeling shows that ITD tuning depends strongly on whether the monaural inputs are spectrotemporally matched, an effect that may generalize to mammals. We compare the spectrotemporal selectivity of monaural inputs of ITD detector neurons in vivo, demonstrating that their selectivity matches. Finally, we show that this refinement can develop through spike timing-dependent plasticity. Our findings raise the unexplored issue of time-dependent frequency tuning in auditory coincidence detectors and offer a unifying perspective.barn owl | nucleus laminaris I nteraural time difference (ITD) is a primary cue for detecting the horizontal position of a sound source (1, 2). The most prevalent model for the mechanism underlying ITD sensitivity assumes that it is created by a circuit of neural delay lines and coincidence detector neurons (3-6). In this model, coincidence detector neurons respond when the left and right ear inputs arrive nearly simultaneously. The temporal delays of the left and right ear inputs created by axonal delay lines determine the neuron's best ITD. An alternative theory retains the coincidence detectors responding to delayed binaural inputs, but postulates cochlear delays instead (7). Experimental evidence in birds does not support this alternative theory (8-10), although some studies in mammals are consistent with it (11). In mammals, ITD sensitivity is thought to be established by the timing of both excitatory and inhibitory inputs (12).A fundamental question these models raise is whether the monaural inputs to the binaural coincidence detector neurons differ only in their timing. Though current evidence is consistent with identical bilateral input shifted in time (5, 8-10, 13), analyses have not taken into account the selectivity of early auditory neurons for the time-dependent spectral structure of sound, which can arise in the auditory nerve.In the mammalian auditory nerve, neurons display a change of preferred instantaneous frequency with time (14-17). This response property is characterized by an instantaneous frequency (IF) glide in the neuron's impulse response. IF glides are also seen in the local field potentials in the owl's nucleus laminaris (NL) (18). It is unknown whether neurons in NL or medial superior olive (MSO), the first binaural nuclei in the avian and mammalian ITD processing pathways, respectively, are selective for these spectrotemporal features and how such selectivity may affect the processing of ITD (4-6). He...

Reverse Correlation Analysis of Auditory-Nerve Fiber Responses to Broadband Noise in a Bird, the Barn Owl

“…2B). At first glance, impulse responses looked similar to what has been reported in the past (de Boer and de Jongh 1978;Carney and Yin 1988;Recio-Spinoso et al 2005;Fischer et al 2011;Fontaine et al 2013): They consisted of a high-frequency oscillation (at around the best frequency of the neuron) modulated in time by an envelope that rose and decayed in a few milliseconds. We fitted analytical functions called gamma chirps to the portion of the STAs where the envelope was higher than 5 % of the maximum, as previously reported (Wagner et al 2009;Fischer et al 2011;Fontaine et al 2013).…”

“…We fitted the resulting STAs to analytical functions called gammachirps (Wagner et al 2009;Fischer et al 2011;Fontaine et al 2013Fontaine et al , 2014. The functions consisted in the product of a high-frequency chirp with a gamma envelope.…”

“…The first one was based on measurements reported in the auditory nerve of cats. Its instantaneous frequency increases linearly with time (Carney et al 1999;Fischer et al 2011); we refer to it as the linear gammachirp GC lin :…”

“…Because the result of the fitting procedure is noiseless, we used it for the analysis as previously reported (Wagner et al 2009;Fischer et al 2011;Fontaine et al 2013). Even though the complex fits were a linear combination of simple time signals, properties of interest such as frequency tuning (Fig.…”

“…Indeed, even if the Fourier transform was linear, its features phase and instantaneous frequency were not. Therefore, the parameters found by the fitting could not be directly used as previously done (Wagner et al 2009;Fischer et al 2011;Fontaine et al 2013), but the corresponding properties had to be computed numerically. Examples of different features studied in this paper are shown in Figure 2.…”