The precedence effect in spatial hearing manifests in cortical neural population responses

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, the main relay point between the inner ear and the auditory cortex, or used modeling of cochlear auditory transduction 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 previously developed to quantify the precedence effect in human 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 interaural time differences 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 early processing mechanisms in the cochlea 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 the auditory cortex, but robust and consistent precedence effects are observable only in the auditory cortex at the level of cortical population responses. This indicates that the precedence effect emerges at later cortical processing stages and is a significantly “higher order” feature than has hitherto been assumed.

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

“…Why our rats exhibit much better ITD performance than that previously reported in biCI users is not yet clear, 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. It is difficult to completely rule out species differences, but this explanation nevertheless seems unlikely given the numerous studies that indicate that rats are a good animal model for human cochlear implantation [11; 63-69] and binaural hearing [11; 28; 29]. We were able to demonstrate that rats have excellent ITD sensitivity with thresholds very similar to those seen in other mammals [28], and exhibit a similar precedence effect, with strikingly similar temporal weighting functions to those seen in humans [29].…”

“…The fact that ITD discrimination is generally better for stimuli with rapid onsets rather than slowly rising envelopes is perhaps unsurprising given that, for normal hearing subjects, onset ITDs are normally the most salient [29; 30]. Electrophysiological studies of ITD sensitivity have similarly demonstrated the importance of onset cues in ITD sensitivity [29; 50; 51]. For example, in the inferior colliculus, ITD sensitivity may drop by 24-48% when onset responses are excluded from the analysis [50].…”

“…Based on previous studies in CI listeners [4; 8; 9] and electrophysiology studies in CI animals [19; 33-37] 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 pulse trains were presented with gently rising slopes (Hanning windowed), rather than sharp onset rectangle windowed pulse trains, given that previous physiological and behavioral studies have consistently shown that ITD sensitivity is heavily weighted towards the onset of stimuli [29; 30]. But gently rising windows make the exact onset of the sound uncertain due to the initially very low amplitude.…”

“…While concerns of species differences remain, there is more and more evidence from recent studies [28; 29] suggesting rat binaural hearing is in fact far more similar to that of humans than previously suspected. In fact, normal hearing rats exhibit behavioral high frequency (“envelope”) ITD thresholds which are very similar to those seen in humans [28], and even show very similar “precedence effects’’ as are seen in human ITD perception [29; 30].…”

“…While concerns of species differences remain, there is more and more evidence from recent studies [28; 29] suggesting rat binaural hearing is in fact far more similar to that of humans than previously suspected. In fact, normal hearing rats exhibit behavioral high frequency (“envelope”) ITD thresholds which are very similar to those seen in humans [28], and even show very similar “precedence effects’’ as are seen in human ITD perception [29; 30]. Thus, the available psychoacoustic data show that the performance parameters of binaural hearing in rats are fundamentally similar to those of humans, and the parsimonious assumption that the functional organisation and underlying anatomy and physiology will be fundamentally similar is valid in the absence of evidence to the contrary.…”