Across all sensory modalities, the effect of context-dependent neural adaptation can be observed at every level, from receptors to perception. Nonetheless, it has long been assumed that the processing of interaural time differences, which is the primary cue for sound localization, is nonadaptive, as its outputs are mapped directly onto a hard-wired representation of space. Here we present evidence derived from in vitro and in vivo experiments in gerbils indicating that the coincidence-detector neurons in the medial superior olive modulate their sensitivity to interaural time differences through a rapid, GABA(B) receptor-mediated feedback mechanism. We show that this mechanism provides a gain control in the form of output normalization, which influences the neuronal population code of auditory space. Furthermore, psychophysical tests showed that the paradigm used to evoke neuronal GABA(B) receptor-mediated adaptation causes the perceptual shift in sound localization in humans that was expected on the basis of our physiological results in gerbils.

Traditionally, the auditory system is thought to serve reliable sound localization. Stimulus-history driven feedback circuits in the early binaural pathway, however, contradict this canonical concept and raise questions about their functional significance. Here we show that stimulus-history dependent changes in absolute space perception are poorly captured by the traditional labeled-line and hemispheric-difference models of auditory space coding. We therefore developed a new decoding model incorporating recent electrophysiological findings in which sound location is initially computed in both brain hemispheres independently and combined to yield a hemispherically balanced code. This model closely captures the observed absolute localization errors caused by stimulus history, and furthermore predicts a selective dilation and compression of perceptional space. These model predictions are confirmed by improvement and degradation of spatial resolution in human listeners. Thus, dynamic perception of auditory space facilitates focal sound source segregation at the expense of absolute sound localization, questioning existing concepts of spatial hearing.

Interaural time differences (ITDs) are the primary cue for the localization of low-frequency sound sources in the azimuthal plane. For decades, it was assumed that the coding of ITDs in the mammalian brain was similar to that in the avian brain, where information is sparsely distributed across individual neurons, but recent studies have suggested otherwise. In this study, we characterized the representation of ITDs in adult male and female gerbils. First, we performed behavioral experiments to determine the acuity with which gerbils can use ITDs to localize sounds. Next, we used different decoders to infer ITDs from the activity of a population of neurons in central nucleus of the inferior colliculus. These results show that ITDs are not represented in a distributed manner, but rather in the summed activity of the entire population. To contrast these results with those from a population where the representation of ITDs is known to be sparsely distributed, we performed the same analysis on activity from the external nucleus of the inferior colliculus of adult male and female barn owls. Together, our results support the idea that, unlike the avian brain, the mammalian brain represents ITDs in the overall activity of a homogenous population of neurons within each hemisphere.

Our sensory environment changes constantly. Accordingly, neural systems continually adapt to the concurrent stimulus statistics to remain sensitive over a wide range of conditions. Such dynamic range adaptation (DRA) is assumed to increase both the effectiveness of the neuronal code and perceptual sensitivity. However, direct demonstrations of DRA-based efficient neuronal processing that also produces perceptual benefits are lacking. Here, we investigated the impact of DRA on spatial coding in the rodent brain and the perception of human listeners. Complex spatial stimulation with dynamically changing source locations elicited prominent DRA already on the initial spatial processing stage, the Lateral Superior Olive (LSO) of gerbils. Surprisingly, on the level of individual neurons, DRA diminished spatial tuning because of large response variability across trials. However, when considering single-trial population averages of multiple neurons, DRA enhanced the coding efficiency specifically for the concurrently most probable source locations. Intrinsic LSO population imaging of energy consumption combined with pharmacology revealed that a slow-acting LSO gain-control mechanism distributes activity across a group of neurons during DRA, thereby enhancing population coding efficiency. Strikingly, such “efficient cooperative coding” also improved neuronal source separability specifically for the locations that were most likely to occur. These location-specific enhancements in neuronal coding were paralleled by human listeners exhibiting a selective improvement in spatial resolution. We conclude that, contrary to canonical models of sensory encoding, the primary motive of early spatial processing is efficiency optimization of neural populations for enhanced source separability in the concurrent environment.

Auditory feedback plays an important role in vocal learning and, more generally, in fine-tuning the acoustic features of communication signals. So far, only a few studies have assessed the developmental onset of auditory feedback. The Lombard effect, a well-studied audiovocal phenomenon, refers to an increase in vocal loudness of a subject in response to an increase in background noise. Here, we studied the time course of the Lombard effect in developing bats, Phyllostomus discolor. We show that infant bats produced louder vocalizations in noise than in silence at an age of only 2 weeks. In contrast, the infant bats' morphology and vocalizations changed gradually until 2 months of age. Furthermore, we found that the Lombard magnitude, i.e. how much the bats increased their vocal loudness in noise relative to silence, correlated positively with the age of the infant bats. We conclude that the Lombard effect features an early developmental origin, indicating a fast maturation of the underlying neural circuits for audio-vocal feedback.

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In natural environments our auditory system is exposed to multiple and diverse signals of fluctuating amplitudes. Therefore, to detect, localize, and single out individual sounds the auditory system has to process and filter spectral and temporal information from both ears. It is known that the overall sound pressure level affects sensory signal transduction and therefore the temporal response pattern of auditory neurons. We hypothesize that the mammalian binaural system utilizes a dynamic mechanism to adjust the temporal filters in neuronal circuits to different overall sound pressure levels. Previous studies proposed an inhibitory mechanism generated by the reciprocally coupled dorsal nuclei of the lateral lemniscus (DNLL) as a temporal neuronal-network filter that suppresses rapid binaural fluctuations. Here we investigated the consequence of different sound levels on this filter during binaural processing. Our in vivo and in vitro electrophysiology in Mongolian gerbils shows that the integration of ascending excitation and contralateral inhibition defines the temporal properties of this inhibitory filter. The time course of this filter depends on the synaptic drive, which is modulated by the overall sound pressure level and N-methyl-D-aspartate receptor (NMDAR) signaling. In psychophysical experiments we tested the temporal perception of humans and show that detection and localization of two subsequent tones changes with the sound pressure level consistent with our physiological results. Together our data support the hypothesis that mammals dynamically adjust their time window for sound detection and localization within the binaural system in a sound level dependent manner.

Detection and localization of a target sound in the presence of concurrent, spatially distributed masking sounds is one of the most challenging tasks for the mammalian auditory system. Previous studies demonstrated that the ability to localize signals is decreased by interfering noise. In order to directly compare the behavioral performance in a signal processing task in noise between gerbils and humans in the free sound field, we quantified their localization ability for a lowfrequency signal in the presence of six masking noise sources surrounding the subject. Thresholds were measured both for masking noises that were correlated or uncorrelated across the masking sources. Overall, the gerbils required a higher signal/noise ratio to detect the low-frequency signal than the humans; that is, the behavioral performance of the gerbils was considerably worse than that of the humans. Moreover, switching from maskers that were uncorrelated across the masking sources to correlated maskers resulted in more masking in gerbils but in a release from masking in humans. These results would suggest that the gerbil may not be a good animal model for binaural processing. However, simulations of the localization thresholds in a numerical model of binaural processing in gerbils and humans reveal that both the inferior overall performance in gerbils and the opposite effect of masker correlation on the detection thresholds can be attributed to the smaller head size and the wider peripheral auditory filters in gerbils. Thus, the current data indicate that the binaural processor itself (i.e., the evaluation of signals coming from the two ears) is equally sensitive in gerbils and humans. However, the physical limitations imposed by the small head prevent the gerbil from performing equally well in the current paradigm.