Generating Synchrony from the Asynchronous: Compensation for Cochlear Traveling Wave Delays by the Dendrites of Individual Brainstem Neurons

Abstract

Broadband transient sounds, such as clicks and consonants, activate a traveling wave in the cochlea. This wave evokes firing in auditory nerve fibers that are tuned to high frequencies several milliseconds earlier than in fibers tuned to low frequencies. Despite this substantial traveling wave delay, octopus cells in the brainstem receive broadband input and respond to clicks with submillisecond temporal precision. The dendrites of octopus cells lie perpendicular to the tonotopically organized array of auditory nerve fibers, placing the earliest arriving inputs most distally and the latest arriving closest to the soma. Here, we test the hypothesis that the topographic arrangement of synaptic inputs on dendrites of octopus cells allows octopus cells to compensate the traveling wave delay. We show that in mice the full cochlear traveling wave delay is 1.6 ms. Because the dendrites of each octopus cell spread across about one third of the tonotopic axis, a click evokes a soma directed sweep of synaptic input lasting 0.5 ms in individual octopus cells. Morphologically and biophysically realistic, computational models of octopus cells show that soma-directed sweeps with durations matching in vivo measurements result in the largest and sharpest somatic excitatory postsynaptic potentials (EPSPs). A low input resistance and activation of a low-voltage-activated potassium conductance that are characteristic of octopus cells are important determinants of sweep sensitivity. We conclude that octopus cells have dendritic morphologies and biophysics tailored to accomplish the precise encoding of broadband transient sounds.

Central Gain Restores Auditory Processing following Near-Complete Cochlear Denervation

“…This remarkable high speed processing is supported by unique synaptic architecture, inhibitory circuitry, and biophysical specializations not found at higher auditory centers (Lu et al, 2008; Mathews et al, 2010; McGinley et al, 2012). What higher auditory neurons lack in specialized high-speed decoding, they make up for in intrinsic and synaptic properties that maintain plasticity well into adulthood.…”

“…Neural circuits in the auditory periphery and brainstem feature remarkable biophysical and synaptic specializations that support acoustic feature extraction with temporal precision on the order of tens of microseconds (Lu et al, 2008; Mathews et al, 2010; McGinley et al, 2012). High-fidelity sound representations at early stages of auditory processing are reformatted as abstractions of the source signal in higher centers (Atencio et al, 2012; Pasley et al, 2012; Rabinowitz et al, 2013; Wang et al, 2008).…”

Predicting spike timing in highly synchronous auditory neurons at different sound levels

“…detailed quantitative models of the AN response (Sumner et al 2003;Zhang et al 2001;Zilany et al 2009) and of cellular models of neurons of the CN (Kuhlmann et al 2002;McGinley et al 2012;Rothman and Manis 2003;Zhang and Carney 2005). While these models provide valuable insight into the underlying mechanisms, they were designed to account for a number of properties of AN fibers or of bushy cells but not to reproduce the precise spike trains in response to arbitrary input sounds.…”

Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources

“…Octopus cells extract information from many (>60 in mice) fibers tuned to a broad range of frequencies [11, 12], each of which activates only a small conductance (<2 nS in mice) and produces a very small (<3 mV in mice) EPSP. They signal the presence of the onset of broadband sounds with extraordinary temporal precision [13–15], projecting to the contralateral SPON [16, 17] and to the columnar area of the VNLL [16, 18, 19] (Fig.…”