On the localization of complex sounds: temporal encoding based on input-slope coincidence detection of envelopes

Abstract

Behavioral and neural findings demonstrate that animals can locate low-frequency sounds along the azimuth by detecting microsecond interaural time differences (ITDs). Information about ITDs is also available in the amplitude modulations (i.e., envelope) of high-frequency sounds. Since medial superior olivary (MSO) neurons encode low-frequency ITDs, we asked whether they employ a similar mechanism to process envelope ITDs with high-frequency carriers, and the effectiveness of this mechanism compared with the process of low-frequency sound. We developed a novel hybrid in vitro dynamic-clamp approach, which enabled us to mimic synaptic input to brain-slice neurons in response to virtual sound and to create conditions that cannot be achieved naturally but are useful for testing our hypotheses. For each simulated ear, a virtual sound, computer generated, was used as input to a computational auditory-nerve model. Model spike times were converted into synaptic input for MSO neurons, and ITD tuning curves were derived for several virtual-sound conditions: low-frequency pure tones, high-frequency tones modulated with two types of envelope, and speech sequences. Computational models were used to verify the physiological findings and explain the biophysical mechanism underlying the observed ITD coding. Both recordings and simulations indicate that MSO neurons are sensitive to ITDs carried by spectrotemporally complex virtual sounds, including speech tokens. Our findings strongly suggest that MSO neurons can encode ITDs across a broad-frequency spectrum using an input-slope-based coincidence-detection mechanism. Our data also provide an explanation at the cellular level for human localization performance involving high-frequency sound described by previous investigators.

Roles for Coincidence Detection in Coding Amplitude-Modulated Sounds

“…Interplay between KLVA and sodium inactivation may further narrow the coincidence window [ 77 ]. In addition, KLVA conductance plays a major role in sensing the rising slope of synchronized synaptic inputs (VCN [ 78 ]; MSO [ 79 ]). Future dynamic clamp experiments in vitro , for example, might reveal more detailed relations between the higher-level coincidence parameters and the underlying membrane and synaptic factors.…”

A low-threshold potassium current enhances sparseness and reliability in a model of avian auditory cortex

“…In many of the auditory areas in the hindbrain and midbrain, nonlinear neural dynamics profoundly affect how a variety of low-level acoustic features are encoded (Carr and Soares, 2002; Khurana et al, 2011; Gai et al, 2014) . For example, neurons that express a low-threshold potassium current ( I K LT ) produce highly phasic responses, responding to rapid increases in excitation but not to slow or steady-state depolarizations (Rothman and Manis, 2003; Gai et al, 2009) .…”

“…For example, neurons that express a low-threshold potassium current ( I K LT ) produce highly phasic responses, responding to rapid increases in excitation but not to slow or steady-state depolarizations (Rothman and Manis, 2003; Gai et al, 2009) . These dynamics are critical to temporal precision in sound localization circuits (Carr and MacLeod, 2010; Gai et al, 2014) and can enhance signal detection in noisy conditions (Svirskis et al, 2002) . Could intrinsic dynamics also contribute to sensory processing at cortical levels?…”

Sensitivity to Interaural Time Differences Conveyed in the Stimulus Envelope: Estimating Inputs of Binaural Neurons Through the Temporal Analysis of Spike Trains

“…Nevertheless, although valid to a first approximation, the dichotomy suggested by the duplex theory is not strict. In particular, human listeners are also sensitive to ITDs conveyed in the modulated stimulus envelope of high-frequency sounds (e.g., Henning 1974), sensitivity also evident in the responses of neurons in the lateral superior olive (LSO; Joris and Yin 1995), inferior colliculus (IC;Yin et al 1984), and, albeit less prominently, the medial superior olive (MSO;Joris 1996;Gai et al 2014). While sensitivity to envelope ITDs is likely less relevant to acoustic hearing (e.g., Devore and Delgutte 2010), it is of higher importance for users of bilateral cochlear implants (CIs)-an increasingly common class of listeners for whom perception of sound is generated by implanted electrical devices that convey acoustic information direct to auditory nerve fibers as a series of modulated electrical pulses.…”