Auditory brainstem models: KV1 ion-channels and depleting end-bulb synapses improve spatial encoding in reverberation

Listeners perceive sound-energy as originating from the direction of its source, even as the direct sound is followed only milliseconds later by reflected sound from multiple different directions. Auditory neural adaptation, before spatial information is binaurally encoded in the brainstem, is suggested as a contributing mechanism, yet the form of sufficient adaptive mechanisms remains unspecified. Though a strong preference for spatial information conveyed in early-arriving sound is observed behaviourally and neurophysiologically, investigation by simultaneously recording from binaural brainstem neurons and their monaural input neurons while controlling adaptation is yet unrealised. Therefore, here we computationally model connected neurons across the auditory brainstem, exploring two biophysical mechanisms that can account for the brainstem’s emphasis of early-arriving spatial information. Matching responses in the medial superior olive (MSO), of neurons encoding interaural time differences, we demonstrate that accurate localisation in reverberant environments is enhanced by realistic pre- and post-synaptic specialisations. Short-term synaptic plasticity at the inputs from auditory nerve fibres to spherical bushy cells (SBCs) in the ventral cochlear nuclei that project bilaterally to the MSO, and Kv1 ion-channels in the SBCs and MSO neurons, promote encoding of reliable spatial information, by suppressing responses to late-arriving sound, particularly at frequencies where reverberant sound is relatively intense in outdoor environments. Suiting weak reverberation outdoors at very low sound frequencies, weak KV1 activity at 200 Hz promotes accurate localisation. Applied to the lateralisation of human speech near 600 Hz in a virtual reverberant room, identical synaptic depression and strong KV1 activity at this higher frequency enhance correct, over spurious, localisation cues at the earliest stages of spatial processing. Author Summary Aurally locating a talker in a reverberant room is often challenging for hearing-impaired listeners. Sound arriving directly from the talker isn’t easily distinguished from reverberant sound reflecting off walls milliseconds later. Nevertheless, normal-hearing listeners easily localise sound-sources, aurally “glimpsing” the reliable spatial information of direct sound during early, rising portions of modulated sounds, while subconsciously ignoring later-arriving, confounding information corrupted by reverberation. Understanding the successful underlying mechanisms may suggest approaches to improve auditory spatial information provided to listeners with hearing aids and cochlear implants. In the auditory brainstem, binaural neurons of the medial superior olive (MSO) preferentially respond to early-arriving spatial information. As simultaneous recordings from MSO neurons and their monaural input neurons while controlling adaptation remain unrealised, to understand the contributing mechanisms, here we identify and computationally demonstrate two mechanisms that suppress responses to late-arriving sound, ultimately emphasising early-arriving sound, and enhancing the localisation of talkers despite reverberation: synaptic depletion in the bilateral cochlear nuclei that drive the MSO, and KV1 ion-channels which support the encoding of spatial information in MSO neurons. Our models reflect the frequency-dependent behavioural emphasis of reliable, early-arriving auditory spatial information, demonstrating brain mechanisms that suppress unreliable spatial information by spectro-temporally opposing typical outdoor reverberation.