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

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 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 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.