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.

The song control nuclei of the zebra finch brain contain more neurones of larger diameter in the male than in the female. This sexual dimorphism is thought to result from differential growth of neurones in the two sexes. Using neurohistological techniques and radioactive tracers, we have studied the development of several forebrain nuclei involved in the control of song and find that the dimorphism arises from neuronal atrophy and death in the female brain as well as from an increase in cell-body size and afferent terminals from other forebrain nuclei in the male. Although the timing of these events varies from nucleus to nucleus, the sequence is essentially similar in all of them except area X. Here we describe the events in one of these nuclei, the robust nucleus of archistriatum (RA), as an example.

Auditory units that responded to sound only when it originated from a limited area of space were found in the lateral and anterior portions of the midbrain auditory nucleus of the owl (Tyto alba). The areas of space to which these units responded (their receptive fields) were largely independent of the nature and intensity of the sound stimulus. The units were arranged systematically within the midbrain auditory nucleus according to the relative locations of their receptive fields, thus creating a physiological map of auditory space.

The cochiear nucleus of the barn owl is composed of two anatomically distinct subnuclei, n, magnocellularis (the magnocellular nucleus) and n. angularis (the angular nucleus). In the magnocellular nuc!eus, a&urQriS tend to respond at a particular phase of a stimuhls xine wave, Phase locking was observed for frequencies up to 9.0 k#z. The intensity-spike count functions of magnocellular units are characterized by high rates of spontaneous act&y, a narrow range of intensities over which spike cnunta changed from spontaneous to saturation levelx, and a small increase in spike counts with intensity over that range. In the angular nucleus, neurons showed little or no tendency to respond at a certain sinusoidal phase, although some showed weak phase IQCking fQr frequencies below :3,% k&c h@dar UnitS t~ically had !ow spontaneous rates, large dynamic ranges, and large increaaea in spike counts with intensityt, reSulting in high satllration levels. The clear difference between the twcl nucki in sensitivity TV both phase and intensity and the reciprocity in response properties support. the hypothesis that each nucleus is speriaiized to process one parameter (phase or intensity) and not the other.

The male zebra finch sings, whereas the female does not. This behavioral dimorphism is correlated with the presence of morphological sex differences within the neural substrate that mediates this behavior, the song system. When a female chick is exposed to 17beta-estradiol her song system is subsequently masculinized. Either testosterone or 5alpha-dihydrotestosterone may then induce such a female to sing when an adult.

Birdsong is a learned behavior controlled by a distinct set of brain nuclei. The song nuclei known as area X, the medial nucleus ofthe dorsolateral thalamus (DLM), and the lateral magnocellular nucleus of the anterior neostriatum (L-MAN) form a pathway that plays an important but unknown role in song learning. One function served by this circuit might be auditory feedback, which is critical to normal song development. We used single unit recordings to demonstrate that all three of these nuclei contain auditory neurons in adult male zebra rmches (Taeniopygia gulata). These neurons are song selective: they respond more robustly to the bird's own song than to songs of conspecific individuals, and they are sensitive to the temporal structure of song. Auditory neurons so highly specialized for song within a pathway required for song learning may play a role in the auditory feedback essential in song development. Recordings in the robust nucleus of the archistriatum (RA), the nucleus to which L-MAN projects, showed that RA also contains highly song-selective neurons. RA receives a direct projection from the caudal nucleus of the ventral hyperstriatum (HVc) as well as from L-MAN. We investigated the contributions of these two inputs to auditory responses of RA neurons by selectively inactivating one or both inputs. Our results suggest that there is a song-selective pathway directly from HVc to RA in addition to the circuit via L-MAN. Thus the songbird brain contains multiple auditory pathways specialized for song, and these circuits may vary in their functional importance at different stages of learning.

This paper investigates the role of the central nucleus of the barn owl's inferior colliculus in determination of the sound-source azimuth. The central nucleus contains many neurons that are sensitive to interaural time difference (ITD), the cue for azimuth in the barn owl. The response of these neurons varies in a cyclic manner with the ITD of a tone or noise burst. Response maxima recur at integer multiples of the period of the stimulating tone, or, if the stimulus is noise, at integer multiples of the period corresponding to the neuron's best frequency. Such neurons can signal, by means of their relative spike rate, the phase difference between the sounds reaching the left and right ears. Since an interaural phase difference corresponds to more than one ITD, these neurons represent ITD ambiguously. We call this phenomenon phase ambiguity. The central nucleus is tonotopically organized and its neurons are narrowly tuned to frequency. Neurons in an array perpendicular to isofrequency laminae form a physiological and anatomical unit; only one ITD, the array-specific ITD, activates all neurons in an array at the same relative level. We, therefore, may say that, in the central nucleus, an ITD is conserved in an array of neurons. Array-specific ITDs are mapped and encompass the entire auditory space of the barn owl. Individual space-specific neurons of the external nucleus, which receive inputs from a wide range of frequency channels (Knudsen and Konishi, 1978), are selective for a unique ITD. Space-specific neurons do not show phase ambiguity when stimulated with noise (Takahashi and Konishi, 1986). Space-specific neurons receive inputs from arrays that are selective for the same ITD. The collective response of the neurons in an array may be the basis for the absence of phase ambiguity in space-specific neurons.

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