Abstract
Locomotion generates adventitious sounds which enable detection and localization of predators and prey. Such sounds contain brisk changes or transients in amplitude. We investigated the hypothesis that ill-understood temporal specializations in binaural circuits subserve lateralization of such sound transients, based on different time of arrival at the ears (interaural time differences, ITDs). We find that Lateral Superior Olive (LSO) neurons show exquisite ITD-sensitivity, reflecting extreme precision and reliability of excitatory and inhibitory postsynaptic potentials, in contrast to Medial Superior Olive neurons, traditionally viewed as the ultimate ITD-detectors. In vivo, inhibition blocks LSO excitation over an extremely short window, which, in vitro, required synaptically evoked inhibition. Light and electron microscopy revealed inhibitory synapses on the axon initial segment as the structural basis of this observation. These results reveal a neural vetoing mechanism with extreme temporal and spatial precision and establish the LSO as the primary nucleus for binaural processing of sound transients.
Highlights
A key component of the neuron doctrine is the unidirectional propagation of action potentials, formulated as the ‘law of dynamic polarization’ by Cajal and van Gehuchten (Berlucchi, 1999; Shepherd, 1991)
Cells for which the trough was lower than 0.5 sp/click (LSO) or the peak was higher than 0.5 sp/click (MSO) were included
Our data lead to a new view of brainstem binaural processing, departing strongly from the previously accepted roles of the MSO as a timing comparator and the Lateral Superior Olive (LSO) as an intensity comparator
Summary
A key component of the neuron doctrine is the unidirectional propagation of action potentials, formulated as the ‘law of dynamic polarization’ by Cajal and van Gehuchten (Berlucchi, 1999; Shepherd, 1991). As the site where action potentials are typically initiated, the axon initial segment (AIS) has a pivotal role in this process (Bender and Trussell, 2012; Kole and Brette, 2018; Leterrier, 2018) and is a bottleneck where inhibition can have an ‘outsized’ effect on a neuron’s output, as proposed for chandelier and basket cells (Blot and Barbour, 2014; Nathanson et al, 2019) Disruption of such synapses is associated with severe brain disorders (Wang et al, 2016), but their exact functional role in the normal brain is speculative because physiological studies of these synapses have been limited to in vitro recordings. The classic ‘duplex’ account posits that these two cues operate in different frequency regions: spatial localization is subserved by ITDs for low-frequency and by IIDs for high-frequency sounds (Strutt, 1907)
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