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.