Cellular and molecular mechanisms of avian auditory coincidence detection

Abstract

Sound localization along the horizontal plane begins with comparing sound arrival times at the two ears in the brainstem coincidence detector neurons. Coincidence detectors are functionally as well as morphologically specialized depending on the frequency of sounds that they handle, and the expression of various channel molecules underlies these specializations. Some voltage-gated K⁺ channels determine the acuity of coincidence detection, and are expressed most abundantly in the middle-frequency-coding neurons. Some hyperpolarization-activated channels are dominant in the high-frequency-coding neurons, and enable a delicate modulation of coincidence detection by noradrenalin. Axonal clustering of Na⁺ channels is also frequency-dependent, and optimizes the coincidence detection. This article aims to provide an overview of recent findings in the cellular and molecular mechanisms of auditory coincidence detection in birds.

Introduction

Localizing sound sources is essential for the survival of animals. It enables animals to avoid danger, or to catch their prey. Sound localization along the horizontal plane requires detecting a small time difference in the sound arrivals between the two ears (interaural time difference, ITD) (Klumpp and Eady, 1956, Moiseff and Konishi, 1981). ITDs are extracted by brainstem neurons that act as coincidence detectors of binaural excitatory synaptic inputs (Jeffress, 1948). Although some differences are proposed in the strategy of encoding ITDs between birds and mammals, coincidence detectors play a key role in the extraction of ITDs in both species (Konishi, 2003, McAlpine and Grothe, 2003). Resolution of sound localization is extremely high, and the resolvable angle of sound source separation is less than 30° along the horizontal plane in many species (cat, Casseday and Neff, 1973; rat, Masterton et al., 1975; songbirds, Klump et al., 1986, Park and Dooling, 1991, Klump, 2000). Especially in the human and the barn owl, the resolvable angle is as small as 1° (Mills, 1958, Knudsen and Konishi, 1979), which corresponds to 10 μs and 3 μs of ITDs, respectively. This resolution of time is outstanding, considering the fact that action potentials often have a duration of the order of a millisecond in the brain (Stuart et al., 1997).

Acuity to localize azimuthal sound sources depends on the frequency of sounds. In the human, the acuity is the highest at 1 kHz within the low-frequency band (0.5–1.5 kHz, Mills, 1958). In various avian species, the highest acuity is achieved at the middle range of their audible frequencies (Klump, 2000), for example 4 kHz in the barn owl (Knudsen and Konishi, 1979) and the canary (Park and Dooling, 1991), and 2 kHz in the great tit (Klump et al., 1986). The frequency to provide the highest acuity differs among species, and might be related to the behavior and environment of animals (Marler, 1955, Klump et al., 1986, Park and Dooling, 1991) as well as the properties of the ear and neural pathways. In the auditory system, neurons are tuned to a specific frequency of sound (characteristic frequency, CF), and information is processed separately by frequency-specific neurons (Brugge, 1992, Klump, 2000). Extraction of ITDs is also frequency specific (Carr and Konishi, 1990, Yin and Chan, 1990). To accomplish this frequency-specific task, coincidence detectors are specialized in morphology depending on the CF (Smith and Rubel, 1979). Recently, a series of studies in the chicken have revealed that the coincidence detectors are also specialized functionally at each CF (Kuba et al., 2005, Kuba et al., 2006, Yamada et al., 2005). These specializations include the type and the number of ion channels, and their subcellular localization.

In this article, we summarize recent findings in the cellular and molecular mechanisms of auditory coincidence detection in birds with some reference to mammals. Most of our descriptions are about how chicken coincidence detector neurons can achieve a microsecond order of acuity and how they are functionally specialized depending on the CF.