Precise Temporal Processing in the Gerbil Auditory Brainstem

Sound localization and recognition are two important tasks of the auditory system. Both require accurate processing of temporal cues. Microsecond differences in the arrival time of a sound at the two ears (interaural time differences, ITDs) are the main cue for localizing low frequency sound sources in space. Traditionally, ITDs are thought to be encoded by an array of coincidence-detector neurons, receiving excitatory inputs from the two ears via axons of variable length (“delay lines”), aligned in a topographic map of azimuthal auditory space. Convincing evidence for the existence of such a map in the mammalian ITD detector, the medial superior olive (MSO) is, however, lacking. Equally undetermined is the role of a temporally glycinergic inhibitory input to MSO neurons. Using in vivo recordings from the MSO of the Mongolian gerbil, the present study showed that the responses of ITD-sensitive neurons are inconsistent with the idea of a topographic map of auditory space. Moreover, whereas the maxima of ITD functions were found to be outside, the steepest slope was positioned in the physiologically encountered range of ITDs. Local iontophoretic application of glycine and its antagonist strychnine revealed that precisely-timed glycinergic inhibition plays a critical role in determining the mechanism of ITD tuning, by shifting the slope into the physiological range of ITDs. Natural sounds are modulated in frequency and amplitude and their recognition depends on the analysis of, amongst others, temporal cues. The bat MSO has been shown to be involved in filtering of sinusoidally amplitude modulated (SAM) sounds. This observation led to the assumption that the MSO serves different functions in high and low frequency hearing mammals, namely filtering of temporal cues in high and sound localization in low frequency hearing animals. However, the response to temporally structured sounds has only rarely been investigated in low frequency hearing animals. This study showed that MSO neurons in the gerbil (a rodent that uses ITDs for sound localization) exhibit filter properties in response to the temporal structure of SAM sounds. These results provide evidence for the fact that the MSO in low frequency hearing animals cannot only be linked to temporal processing of spatial cues, but has additional temporal functions. Auditory information is processed in a number of parallel paths in the ascending auditory pathway. At the brainstem level, several structures are involved, which are known to serve different well-defined functions. However, the function of one prominent brainstem nucleus, the rodent superior paraolivary nucleus (SPN) is unknown. Two hypotheses have been tested using extracellular single cell physiology in the gerbil. The existence of binaural inputs indicates that the SPN might be involved in sound localization. Although almost half of the neurons exhibited binaural interactions (most of them excited from both ears), effects of ITDs and interaural intensity differences were weak and ambiguous. Thus, a straightforward function of SPN in sound localization appears to be unlikely. Inputs from octopus and multipolar/stellate cells of the cochlear nucleus, and from principal cells of the medial nucleus of the trapezoid body, could relate to precise temporal processing in the SPN. Based on discharge types, two subpopulations of SPN cells were observed: sustained discharges and phasic ON or OFF responses. The temporal precision of ON responders in response to pure tones and SAM was significantly higher than that in sustained responders. The existence of at least two subpopulations of neurons (ON and sustained responders) is in line with different subsets of SPN cells that can be distinguished morphologically and may point to them having different roles in the processing of temporal sound features.