Novel approaches for the investigation of sound localization in mammals

The ability to localize sounds in space is important to mammals in terms of awareness of the environment and social contact with each other. In many mammals, and particularly in humans, localization of sound sources in the horizontal plane is achieved by an extraordinary sensitivity to interaural time differences (ITDs). Auditory signals from sound sources, which are not centrally located in front of the listener travel different distances to the ears and thereby generate ITDs. These ITDs are first processed by binaural sensitive neurons of the superior olivary complex (SOC) in the brainstem. Despite decades of research on this topic, the underlying mechanisms of ITD processing are still an issue of strong controversy and the processing of concurrent sounds for example is not well understood. Here I used in vivo extra-cellular single cell recordings in the dorsal nucleus of the lateral lemniscus (DNLL) to pursue three novel approaches for the investigation of ITD processing in gerbils, a well-established animal model for sound localization. The first study focuses on the ITD processing of static pure tones in the DNLL. I found that the low frequency neurons of the DNLL express an ITD sensitivity that closely resembles the one seen in the SOC. Tracer injections into the DNLL confirmed the strong direct inputs of the SOC to the DNLL. These findings support the population of DNLL neurons as a suitable novel approach to study the general mechanism of ITD processing, especially given the technical difficulties in recording from neurons in the SOC. The discharge rate of the ITD-sensitive DNLL neurons was strongly modulated over the physiological relevant range of ITDs. However, for the majority of these neurons the maximal discharge rates were clearly outside this range. These findings contradict the possible encoding of physiological relevant ITDs by the maximal discharge of single neurons. In contrast, these data support the more recent hypothesis that the discharge rate averaged over a population of ITD-sensitive neurons encodes the location of low frequency sounds. In the second study, I investigated the ITD processing of two concurrent sound sources, extending the classical approach of using only a single sound source. As concurrent sound sources a pure tone and background noise were chosen. The data show that concurrent white noise has a high impact on the response to tones and vice versa. The discharge rate to tones was mostly suppressed by the noise. The discharge rate to the noise was suppressed or enhanced by the tone depending on the ITD of the tone. Investigating the responses to monaural stimulation and to tone stimulation with concurrent spectrally filtered noise, I found that the ITD sensitivity of DNLL neurons strongly depends on the spectral compositions, the ITDs, and the levels of the concurrent sound sources. Two different mechanisms that mediate these findings were identified: monaural across-frequency interactions and temporal interactions at the level of the coincidence detector. Simulations of simple coincidence detector models (in cooperation with Christian Leibold) suggested this interpretation. In the third study of my thesis, the temporal resolution of binaural motion was analyzed. Particularly, it was investigated how fast the neuronal system can follow changes of the ITD. Here, psychophysical experiments in humans and electrophysiological recordings in the gerbil DNLL were performed using identical acoustic stimulation. Although the binaural system has previously been described as sluggish, the binaural response of ITD-sensitive DNLL neurons was found to follow fast changes of ITDs. Furthermore, in psychophysical experiments in humans, the binaural performance was better than expected when using a novel plausible motion stimulus. These data suggest that the binaural system can follow changes of the binaural cues much faster than previously reported and almost as fast as the monaural system, given a physiological useful stimulus. In summary, the results presented here establish the ITD-sensitive DNLL neurons as a novel approach for the investigation of ITD processing. In addition, the usage of more complex and naturalistic stimuli is a promising and necessary approach for opening the field for further studies regarding a better understanding of the hearing process.