Echo delay versus spectral cues for temporal hyperacuity in the big brown bat, Eptesicus fuscus.

Big brown bats can discriminate between echoes that alternate in delay (jitter) by as little as 10-15 ns and echoes that are stationary in delay. This delay hyperacuity seems so extreme that it has been rejected in favor of an explanation in terms of artifacts in echoes, most likely spectral in nature, that presumably are correlated with delay. Using different combinations of digital, analog, and cable delays, we dissociated the overall delay of jittering echoes from the size of the analog component of delay, which alone is presumed to determine the strength of the apparatus artifact. The bats' performance remains invariant with respect to the overall delay of the jittering echoes, not with respect to the amount of analog delay. This result is not consistent with the possible use of delay-related artifacts produced by the analog delay devices. Moreover, both electronic and acoustic measurements disclose no spectral cues or impedance-mismatch reflections in delayed signals, just time-delays. The absence of artifacts from the apparatus and the failure of overlap and interference from reverberation to account for the 10-ns result means that closing the gap between the level of temporal accuracy plausibly explained from physiology and the level observed in behavior may require a better understanding of the physiology.

Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats.

The big brown bat, Eptesicus fuscus, navigates and hunts prey with echolocation, a modality that uses the temporal and spectral differences between vocalizations and echoes from objects to build spatial images. Closely spaced surfaces ("glints") return overlapping echoes if two echoes return within the integration time of the cochlea ( approximately 300-400 micros). The overlap results in spectral interference that provides information about target structure or texture. Previous studies have shown that two acoustic events separated in time by less than approximately 500 micros evoke only a single response from neural elements in the auditory brain stem. How does the auditory system encode multiple echoes in time when only a single response is available? We presented paired FM stimuli with delay separations from 0 to 24 micros to big brown bats and recorded local field potentials (LFPs) and single-unit responses from the inferior colliculus (IC). These stimuli have one or two interference notches positioned in their spectrum as a function of two-glint separation. For the majority of single units, response counts decreased for two-glint separations when the resulting FM signal had a spectral notch positioned at the cell's best frequency (BF). The smallest two-glint separation that reliably evoked a decrease in spike count was 6 micros. In addition, first-spike latency increased for two-glint stimuli with notches positioned nearby BF. The N(4) potential of averaged LFPs showed a decrease in amplitude for two-glint separations that had a spectral notch near the BF of the recording site. Derived LFPs were computed by subtracting a common-mode signal from each LFP evoked by the two-glint FM stimuli. The derived LFP records show clear changes in both the amplitude and latency as a function of two-glint separation. These observations in relation with the single-unit data suggest that both response amplitude and latency can carry information about two-glint separation in the auditory system of E. fuscus.

Representation of waveform periodicity in the auditory midbrain of the bullfrog, Rana catesbeiana.

The period of complex signals is encoded in the bullfrog's eighth nerve by a synchrony code based on phase-locked responding. We examined how these arrays of phase-locked activity are represented in different subnuclei of the auditory midbrain, the torus semicircularis (TS). Recording sites in different areas of the TS differ in their ability to synchronize to the envelope of complex stimuli, and these differences in synchronous activity are related to response latency. Cells in the caudal principal nucleus (cell sparse zone) have longer latencies, and show little or no phase-locked activity, even in response to low modulation rates, while some cells in lateral areas of the TS (magnocellular nucleus, lateral part of principal nucleus) synchronize to rates as high as 90-100 Hz. At midlevels of the TS, there is a lateral-to-medial gradient of synchronization ability: cells located more laterally show better phaselocking than those located more medially. Pooled all-order interval histograms from short latency cells located in the lateral TS represent the waveform periodicity of a biologically relevant complex harmonic signal at different stimulus levels, and in a manner consistent with behavioral data from vocalizing male frogs. Long latency cells in the caudal parts of the TS (cell sparse zone, caudal magnocellular nucleus) code stimulus period by changes in spike rate, rather than by changes in synchronized activity. These data suggest that neural codes based on rate processing and time domain processing are represented in anatomically different areas of the TS. They further show that a populationbased analysis can increase the precision with which temporal features are represented in the central auditory system.