The precedence effect in spatial hearing emerges only late in the auditory pathway

Abstract

Background: To localize sound sources accurately in a reverberant environment, human binaural hearing strongly favors analyzing the initial wave front of sounds. Behavioral studies of this 'precedence effect' have so far largely been confined to human subjects, limiting the scope of complementary physiological approaches. Similarly, physiological studies have mostly looked at neural responses in the inferior colliculus, or used modeling of cochlear mechanics in an attempt to identify likely underlying mechanisms. Studies capable of providing a direct comparison of neural coding and behavioral measures of sound localization under the precedence effect are lacking. Results: We adapted a 'temporal weighting function' paradigm for use in laboratory rats. The animals learned to lateralize click trains in which each click in the train had a different interaural time difference. Computing the 'perceptual weight' of each click in the train revealed a strong onset bias, very similar to that reported for humans. Follow-on electrocorticographic recording experiments revealed that onset weighting of ITDs is a robust feature of the cortical population response, but interestingly it often fails to manifest at individual cortical recording sites. Conclusion: While previous studies suggested that the precedence effect may be caused by cochlear mechanics or inhibitory circuitry in the brainstem and midbrain, our results indicate that the precedence effect is not fully developed at the level of individual recording sites in auditory cortex, but robust and consistent precedence effects are observable at the level of cortical population responses. This indicates that the precedence effect is significantly 'higher order' than has hitherto been assumed.

Interaural time difference sensitivity under binaural cochlear implant stimulation persists at high pulse rates up to 900 pps

“…This context makes the recent development of a behavioral biCI rat model (Rosskothen-Kuhl et al 2021) invaluable. Normal hearing rats exhibit behavioral high frequency ("envelope") ITD thresholds which are very similar to those seen in humans (Li et al 2019), and even show very similar "precedence effects" as are seen in human ITD perception (Brown and Stecker 2010;Li et al 2021). This makes rats a well validated model for human binaural hearing, well suited for characterizing the stimulus parameter ranges that allow high levels of ITD sensitivity with high accuracy and reproducibility.…”

“…In addition, better ITD discrimination in stimuli with rapid onsets is perhaps unsurprising given that, for normal hearing subjects, onset ITDs are normally the most salient (Brown and Stecker 2010). Electrophysiological studies of ITD sensitivity have similarly demonstrated the importance of onset cues in ITD sensitivity at least at the level of the inferior colliculus (Buck et al 2021;Haqqee et al 2021;Li et al 2021) with a fall in ITD sensitivity of between 24-48% when onset responses were excluded (Buck et al 2021). Comparable results were also observed in a behavioral study in normal hearing rats across different pulse rates (Li et al 2019).…”

“…Why our rats exhibit much better ITD performance than that previously reported in biCI users is not known, but possible explanations, some of which we have touched on above, include species differences, differences in the nature of the stimulation and/or training effects. Species differences may of course play a role, but a multitude of studies indicate that rats are a good animal model for human cochlear implantation (Rosskothen-Kuhl and Illing 2010; Rosskothen-Kuhl and Illing 2012; Rosskothen-Kuhl and Illing 2014; Rauch et al 2016; Rosskothen-Kuhl et al 2018; Jakob et al 2019; Rosskothen-Kuhl et al 2021; Weltin et al 2022) and binaural hearing (Li et al 2019; Li et al 2021; Rosskothen-Kuhl et al 2021). We thus think species differences are unlikely to be a major factor.…”

“…Based on previous studies in CI listeners (Litovsky et al 2012; Ehlers et al 2017; Thakkar et al 2020) and electrophysiology studies in CI animals (Tillein et al 2009; Hancock et al 2012; Hancock et al 2013; Chung et al 2014; Chung et al 2016; Tillein et al 2016) we expected to see generally better ITD sensitivities for lower pulse rates and a rapid drop off above 300 pps. In addition, we expected to observe reduced ITD lateralization performances when presenting pulse trains with gently rising slopes (Hanning windowed) rather than sharp onset rectangle windowed pulse trains considering previous physiological and behavioral studies on ITDs demonstrating the precedence effect for these binaural spatial cues (Brown and Stecker 2010; Li et al 2021). This study demonstrates these expectations were in part born out in the data, but not nearly as strongly as one might suspect.…”