Update articleCellular and molecular mechanisms of avian auditory coincidence detection
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.
Section snippets
Low-threshold K+ current plays a crucial role in coincidence detection
Extraction of ITDs in birds is explained on the classical Jeffress model (1948), which requires delay lines and an array of coincidence detectors. Delay lines produce delays in the arrival times of action potentials to each coincidence detector, while the coincidence detectors fire maximally when they receive simultaneous synaptic inputs from both ears. These two elements allow each ITD to be encoded as the place of the most active neuron in the array. In birds, ITDs are extracted in the
Acuity of coincidence detection is frequency-dependent
NL is tonotopically organized so that the CF of neurons decreases from the rostro-medial (high CF) to the caudo-lateral (low CF) direction (Rubel and Parks, 1975), and ITDs are determined separately by frequency-specific NL neurons. Kuba et al. (2005) examined the coincidence detection of NL neurons along the tonotopic axis in the chicken. NL neurons were classified into three groups according to the CF (Fig. 2A), and their half-peak width of coincidence detection was measured. The half-peak
Noradrenergic control of coincidence detection
Hyperpolarization-activated cation current (Ih) is another major conductance activated at the rest in NL neurons (Kuba et al., 2002b). Ih has slow activation and deactivation kinetics, and has the reversal potential positive to the resting membrane potential (−50 to −20 mV) (Pape, 1996). These allow Ih to accelerate the EPSPs in two ways. First, it works as a shunting conductance to shorten the membrane time constant. Second, it depolarizes the resting membrane potential and activates IKLT.
Specialization of action potential initiation site along the tonotopic axis
NL neurons are specialized along the tonotopic axis not only in the process of summating EPSPs at the soma and dendrites, but also in the process of initiating action potentials in the axon. Carr and Boudreau (1993) reported in their electron-microscopic studies that the initial segment of NL neurons is myelinated in the chicken and the barn owl. Since the myelination was not observed in low-frequency NL neurons (below 1 kHz), they considered that the myelinated initial segment would be an
Comparison to mammals
MSO neurons have several morphological and biophysical features common to NL neurons (Oertel, 1999, Trussell, 1999). These include bipolar dendrites (Scheibel and Scheibel, 1974), rapid time course of EPSCs (Smith et al., 2000), and large IKLT and Ih conductances (Smith, 1995, Svirskis et al., 2002). Furthermore, channel molecules underlying the synaptic and membrane conductances are also common between MSO and NL (Parks, 2000, Rosenberger et al., 2003, Koch et al., 2004), suggesting that the
Perspective
NL neurons show several functional as well as morphological refinements along the tonotopic axis to enhance the coincidence detection at each frequency. In particular, the high density of Kv1.2 channels enables a submillisecond order of coincidence detection and would contribute to the high resolution of sound localization at the middle-frequency range. The dominance of HCN2 channels allows the high-frequency NL neurons to modulate the acuity of coincidence detection dynamically by
Acknowledgements
I thank Drs. T.M. Ishii and R. Yamada for their contributions. I am deeply grateful to Prof. H. Ohmori for encouragement, collaboration, and discussion. This work was supported by Grants-in-Aid from the MEXT (17700368, 17021021 and 18019016).
References (85)
- et al.
Serotonin augments the cationic current Ih in central neurons
Neuron
(1989) - et al.
An axon with a myelinated initial segment in the bird auditory system.
Brain Res.
(1993) - et al.
Relative abundance of subunit mRNAs determines gating and Ca2+-permeablity of AMPA receptors in principal neurons and interneurons in rat CNS
Neuron
(1995) The analysis of interaural time difference in the chick brain stem
Physiol. Behav.
(2005)- et al.
Cochlear microphonic measurements of interaural time differences in the chick
Hear. Res.
(1994) - et al.
A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick
Brain Res.
(1995) - et al.
A model of spike initiation in neocortical pyramidal neurons
Neuron
(1995) - et al.
Sound localization and delay lines—do mammals fit the model?
Trends Neurosci.
(2003) The AMPA receptors of auditory neurons
Hear. Res.
(2000)- et al.
Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain
Cell
(1998)
Neuropil organization in the superior olive of the cat
Exp. Neurol.
Action potential initiation and propagation in neurons of the mammalian CNS
Trends Neurosci.
The role of dendrites in auditory coincidence detection
Nature
Passive soma facilitates submillisecond coincidence detection in the owl's auditory system
J. Neurophysiol.
Activity of NE-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep–waking cycle
J. Neurosci.
Hyperpolarization-activated cation current (Ih) in neurons of the medial nucleus of the trapezoid body: voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem
J. Neurophysiol.
Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive
Eur. J. Neurosci.
Precise inhibition is essential for microsecond interaural time difference coding
Nature
Effect of GABA on the processing of interaural time differences in nucleus laminaris neurons in the chick
Eur. J. Neurosci.
An overview of central auditory processing
Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways
J. Comp. Neurol.
Axonal delay lines for time measurement in the owl's brainstem
Proc. Natl. Acad. Sci. U.S.A.
A circuit for detection of interaural time differences in the brain stem of the barn owl
J. Neurosci.
Localizatioin of pure tones
J. Acoust. Soc. Am.
Localization of sodium channels in cultured neural cells
J. Neurosci.
Synaptic depression in the localization of sound
Nature
Effects of inhibitory feedback in a network model of avian brain stem
J. Neurophysiol.
Inhibition of the hyperpolarization-activated current (if) induced by acetylcholine in rabbit sino-atrial node myocytes
J. Physiol.
Muscarinic control of the hyperpolarization-activated current (if) in rabbit sino-atrial node myocytes
J. Physiol.
Properties of the hyperpolarizing-activated current (If) in cells isolated from the rabbit sino-atrial node
J. Physiol.
The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system
J. Neurosci.
Tonotopic gradients of membrane and synaptic properties for neurons of the chicken nucleus magnocellularis
J. Neurosci.
The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick
J. Physiol.
Optimal neural population coding of an auditory spatial cue
Nature
Sound localization and use of binaural cues by the gerbil (Meriones unguiculatus)
Behav. Neurosci.
A place theory of sound localization
J. Comp. Physiol. Psychol.
Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study.
Brain Res.
Coincidence detection by binaural neurons in the chick brain stem
J. Neurophysiol.
Sound localization in birds
The great tit's (Parus major) auditory resolution in azimuth
J. Comp. Physiol.
Some measurements of interaural time difference thresholds
J. Acoust. Soc. Am.
Mechanisms of sound localization in the barn owl (Tyto alba)
J. Comp. Physiol.
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