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.

Neurons of the barn owl's (Tyto alba) nucleus laminaris, the first site of binaural convergence, respond in a phase-locked fashion to a tone delivered to either ear. It may take longer to elicit phase-locked spikes from one ear than from the other. This disparity in delay differs from neuron to neuron and is independent of tonal frequency. In binaural stimulation, neurons respond best when sound in one ear leads that in the other by an amount equal to their delay disparities but opposite in sign. This condition causes simultaneous arrival of phaselocked spikes from the two sides. Laminari neurons can thus be described as coincidence detectors. The phase of a toneinduced evoked potential, termed "neurophonic," varies systematically with position in nucleus laminaris. From dorsal to ventral within the nucleus, the phase delay of a contralaterally elicited potential decreases and that of its ipsilateral counterpart increases. Therefore, if the neurophonic delay is due to the delay of phase-locked spikes, an orderly representation ofdelay disparities is shown. Because they act as coincidence detectors, laminaris neurons should show selectivity for interaural phase difference based on their place in the nucleus. Thus, nucleus laminaris presumably measures and maps interaural phase differences by using the principles of delay lines and coincidence detection.Sound localization requires neuronal analysis of binaural cues. The "place theory" of sound localization, proposed originally by Jeffress (1), explains how the auditory system can measure interaural time differences, an important cue for horizontal localization in the barn owl (2). The Jeffress model incorporates the concepts of neural delay lines and coincidence detectors. Binaural neurons form an array along which monaural inputs from the two sides converge. The position of a neuron relative to the ends of the array determines the axonal path length from each side. This, in turn, determines the sign and magnitude of the difference in neural transmission delays from the two sides. If the neuron fires maximally when the neural signals from the two sources arrive simultaneously, it would be most sensitive to an interaural time difference that offsets this difference in neural transmission delays. Thus, a map of neural sensitivity to interaural time difference is generated. Several lines of evidence suggest that this model applies to the owl's nucleus laminaris. MATERIALS AND METHODSBarn owls (Tyto alba) were prepared for electrophysiological recording under Ketamine anesthesia. Glass-coated platinum/iridium electrodes were used for single and multiunit recordings. Electrodes were placed stereotaxically. A PDP 11/40 computer recorded the time of occurrence of amplified and level-discriminated action potentials and stored multiunit potentials digitized at a sampling rate of 25 kHz.Earphones inserted in the external auditory meatus delivered stimuli that consisted oftone bursts 100 msec in duration with a rise and decay time of 5 msec. The earphones were calibr...

1. Single- and multiunit recordings were obtained from neurons in the auditory cortex of the echolocating bat Myotis lucifugus, while trains of stimuli designed to simulate the bat's frequency-modulated (FM) orientation pulse and its returning echo were delivered. It was found that many neurons in the cortex responded selectively to pulse-echo pairs only if the time delay separating the artificial pulse and the echo was within a certain range. This response property is called "delay-dependent facilitation." Since echolating bats are known to utilize echo-delay information for the determination of target distance, it is postulated that these neurons are involved in the process of distance perception. 2. Two types of delay-sensitive neurons were characterized on the basis of their response patterns. P-type units had short maximum response delays, narrow delay response functions, and response latencies for pulse-echo pairs that were similar to their response latencies for single loud FM pulses. E-type units had longer maximum response delays, wide delay response functions, and pulse-echo pair response latencies that were time-locked to the echo. Another important difference between these two classes was that changes in the amplitude of the artificial echo caused systematic changes in the delay response of E-type units but not of P-type units. 3. The sharpness and stability of the delay response functions of P-type units suggested that they may encode target distance by responding at discrete echo delays. In contrast, delay tuning may not be an unambiguous determinant of echo delay in E-type units. Here, the most consistent and reliable response parameter for echo delay is the time at which the responses occurred. This suggested that echo delay could be encoded by the temporal pattern of responses in E-type units in relation to the responses evoked by the outgoing orientation cry. The different range of delay of delay sensitivity of P-type and E-type units indicates that these two mechanisms could be operating at different ranges of target distance. 4. P-type and E-type responses may not be due to different populations of neurons but to different response properties of the same population under different conditions. Evidence for this proposition was obtained by showing that in some recordings, decreases in the amplitude of the artificial pulse caused a switch in response from a long best delay, E-type response to a short best delay, P-type response. This suggested that the delay sensitivity of cortical neurons could be under the bat's control based on the intensity of its pulse emissions.

1. In order to investigate the possible neural mechanisms underlying delay-dependent facilitation in the bat's auditory cortex (18), the responses to single FM pulses of varying amplitude were examined. Analysis of amplitude-spike count functions revealed three distinct types: monotonic, simple nonmonotonic, and complex nonmonotonic. The complex nonmonotonic function had two separate amplitude peaks, with a clear notch or worst amplitude between them. Other units had spike count functions that were mainly monotonic or nonmonotonic, but showed some evidence for a second response region. 2. Examination of response latency revealed another novel response property, which has been termed the paradoxical latency shift. Units with this response property responded at a shorter latency to sounds of low amplitude than to sounds of high amplitude. The paradoxical latency shift also appears to be related to the twin-peaked complex nonmonotonic response function. Units with the most prominent twin-peaked response functions also had the clearest latency shifts. In these units, the high-amplitude peak corresponded to the long-latency response and the low-amplitude peak to the short-latency-response. 3. These curious spike count and latency observations can be explained if they are considered in relation to the temporal and amplitude pattern of the acoustic input during echolocation. In echolocation, a loud orientation pulse is followed by a weaker echo. In delay-dependent facilitation, this pulse-echo sequence is followed by a neural response if the pulse-echo delay is appropriate. The simplest model for delay-dependent facilitation assumes that a synchronization of excitatory inputs from the pulse and echo is needed for facilitation. Since the weaker echo occurs after the pulse, it is closer in time to the postulated synchronization point. Therefore, in order for this model to work, the echo input must reach the summation place with less of a time lag than the pulse input. This is exactly what is seen with the paradoxical latency shift; the loud "pulse" response is delayed relative to the weak "echo" response.

Response patterns of neurons in the cochlear nuclei of the barn owl (Tyto alba) were studied by obtaining poststimulus time histograms (PSTHs) and interspike interval histograms for the response to short tone bursts at the neuron's characteristic frequency. The observed response patterns can be classified according to the scheme developed for neurons of the mammalian cochlear nuclear complex (22). Neurons of the magnocellular cochlear nucleus (n. magnocellularis), which respond in a phase-locked manner to sinusoidal signals and do not show large increases in spike discharge rate with changes in stimulus intensity (26), have "primarylike" (PSTH) discharge patterns and broad interspike interval histograms. This indicates that magnocellular neurons have irregular firing patterns, with the timing of individual spikes being dependent on the phase of the stimulus waveform. Neurons of the angular cochlear nucleus (n. angularis), which show little or no phase-locking and large increases in spike rate with increasing intensity (26), had almost exclusively "transient chopper" discharge patterns. The interspike interval histograms of these angular units are sharp, indicating that their discharge is very regular. At the onset of the response where the chopper pattern is observed, both discharge regularity and rate-intensity sensitivity are at their maximum levels. Several "onset" units were isolated in the angular cochlear nucleus, but no "pauser" or "buildup" units were seen. Also, all of the units in the angular nucleus had monotonic rate-intensity functions. Thus no neural response patterns typical of mammalian dorsal cochlear nucleus units were observed. The relationship of response pattern type to neural function is discussed in relation to the acoustic cues used by the owl for two-dimensional sound localization. The primarylike, phase-locked discharge of magnocellular units is undoubtedly involved in the analysis of interaural differences in stimulus phase, which the owl uses for horizontal localization. There is strong evidence suggesting that the angular nucleus is involved in processing stimulus intensity information, which is important for determining sound elevation (due to asymmetries in vertical directionality of the owl's external ears). The predominant chopper patterns seen in the angular nucleus suggest that in the owl, this response type is correlated with stimulus intensity processing. Similarities in both anatomy and physiology suggest that the magnocellular nucleus is analogous to the spherical cell or bushy cell population of the anterior division of the mammalian anteroventral cochlear nucleus.(ABSTRACT TRUNCATED AT 400 WORDS)