Theoretical foundations of the sound analog membrane potential that underlies coincidence detection in the barn owl

Go Ashida,Kazuo Funabiki,Catherine E Carr

doi:10.3389/fncom.2013.00151

Abstract

A wide variety of neurons encode temporal information via phase-locked spikes. In the avian auditory brainstem, neurons in the cochlear nucleus magnocellularis (NM) send phase-locked synaptic inputs to coincidence detector neurons in the nucleus laminaris (NL) that mediate sound localization. Previous modeling studies suggested that converging phase-locked synaptic inputs may give rise to a periodic oscillation in the membrane potential of their target neuron. Recent physiological recordings in vivo revealed that owl NL neurons changed their spike rates almost linearly with the amplitude of this oscillatory potential. The oscillatory potential was termed the sound analog potential, because of its resemblance to the waveform of the stimulus tone. The amplitude of the sound analog potential recorded in NL varied systematically with the interaural time difference (ITD), which is one of the most important cues for sound localization. In order to investigate the mechanisms underlying ITD computation in the NM-NL circuit, we provide detailed theoretical descriptions of how phase-locked inputs form oscillating membrane potentials. We derive analytical expressions that relate presynaptic, synaptic, and postsynaptic factors to the signal and noise components of the oscillation in both the synaptic conductance and the membrane potential. Numerical simulations demonstrate the validity of the theoretical formulations for the entire frequency ranges tested (1–8 kHz) and potential effects of higher harmonics on NL neurons with low best frequencies (<2 kHz).

Highlights

Synchronized neural activity underlies various types of information processing in the brain
In the accompanying paper (Ashida et al, 2013), we systematically examine the roles of the number of converging nucleus magnocellularis (NM) fiber on the nucleus laminaris (NL) neuron, their average spike rate, their degree of phase-locking and the synaptic time constant to investigate how these parameters affect the formation of sound analogue potential in the NL neuron
The sound analogue membrane potential, which is created by a “volley” of phase-locked inputs (Wever and Bray, 1930; Joris and Smith, 2008), underlies coincidence detection in the owl’s NL neurons (Funabiki et al, 2011)

Summary

Introduction

Synchronized neural activity underlies various types of information processing in the brain. A diversity of sensory neurons encode temporal information via phase-locked spiking (Carr and Friedman, 1999). In the auditory brainstems of mammals, reptiles, and birds, neurons involved in sound localization convey precise temporal information of sound using phase-locked spikes (cats: Joris et al, 1994; gerbils: Dehmel et al, 2010; caimans: Carr et al, 2009; owls: Sullivan and Konishi, 1984; Köppl, 1997; chickens: Warchol and Dallos, 1990; Fukui et al, 2006; redwing blackbirds: Sachs and Sinnott, 1978). The degree of phase-locking, measured as the vector strength (VS) (Goldberg and Brown, 1969), is significant for frequencies up to about 8 kHz in the owl’s nucleus magnocellularis (NM) (Sullivan and Konishi, 1984; Köppl, 1997)

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