Detection of interaural time differences underlies azimuthal sound localization in the barn owl Tyto alba. Axons of the cochlear nucleus magnocellularis, and their targets in the binaural nucleus laminaris, form the circuit responsible for encoding these interaural time differences. The nucleus laminaris receives bilateral inputs from the cochlear nucleus magnocellularis such that axons from the ipsilateral cochlear nucleus enter the nucleus laminaris dorsally, while contralateral axons enter from the ventral side. This interdigitating projection to the nucleus laminaris is tonotopic, and the afferents are both sharply tuned and matched in frequency to the neighboring afferents. Recordings of phase-locked spikes in the afferents show an orderly change in the arrival time of the spikes as a function of distance from the point of their entry into the nucleus laminaris. The same range of conduction time (160 mu sec) was found over the 700-mu m depth of the nucleus laminaris for all frequencies examined (4-7.5 kHz) and corresponds to the range of interaural time differences available to the barn owl. The estimated conduction velocity in the axons is low (3-5 m/sec) and may be regulated by short internodal distances (60 mu m) within the nucleus laminaris. Neurons of the nucleus laminaris have large somata and very short dendrites. These cells are frequency selective and phase-lock to both monaural and binaural stimuli. The arrival time of phase-locked spikes in many of these neurons differs between the ipsilateral and contralateral inputs. When this disparity is nullified by imposition of an appropriate interaural time difference, the neurons respond maximally. The number of spikes elicited in response to a favorable interaural time difference is roughly double that elicited by a monaural stimulus. Spike counts for unfavorable interaural time differences fall well below monaural response levels. These findings indicate that the magnocellular afferents work as delay lines, and the laminaris neurons work as co-incidence detectors. The orderly distribution of conduction times, the predictability of favorable interaural time differences from monaural phase responses, and the pattern of the anatomical projection from the nucleus laminaris to the central nucleus of the inferior colliculus suggest that interaural time differences and their phase equivalents are mapped in each frequency band along the dorsoventral axis of the nucleus laminaris.

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The circuit from the cochlear nucleus magnocellularis to the nucleus laminaris supports the encoding and measurement of interaural time differences in the auditory brainstem. Specializations for the encoding of temporal information include the few and/or short dendrites and thick axons of the magnocellular and laminaris neurons, and the high degree of convergence in the circuit. Magnocellular cells have large cell bodies covered with somatic spines. The cells have few dendrites, and the number of dendrites decreases from low to high best frequency regions of the nucleus. Magnocellular neurons receive both auditory nerve terminals and GABAergic terminals with symmetric synapses and terminals filled with pleomorphic vesicles. The axonal projections of magnocellular neurons to the nucleus laminaris form maps of interaural time difference. About 100 magnocellular afferents from each side converge on each laminaris neuron, and the terminals from each side do not occupy separate domains on the cell. These terminals form punctate asymmetric synapses on both the dendrites and the cell bodies of laminaris neurons. Laminaris neurons also receive GABAergic terminals which form symmetric synapses. Laminaris neurons have oval cell bodies covered with very short dendrites. The cells in the low best frequency region of the nucleus laminaris have longer dendrites.

Precise temporal coding is a hallmark of the auditory system. Selective pressures to improve accuracy or encode more rapid changes have produced a suite of convergent physiological and morphological features that contribute to temporal coding. Comparative studies of temporal coding also point to shared computational strategies, and suggest how selection acts to improve coding. Both the avian cochlear nucleus angularis and the mammalian cochlear nuclei have heterogeneous cell populations, and similar responses to sound. These shared characteristics may represent convergent responses to similar selective pressures to encode features of airborne sound.

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