Microseconds-level coding of echo delay in the auditory brainstem of an FM-echolocating bat

Echolocating big brown bats (Eptesicus fuscus) detect changes in ultrasonic echo delay with an acuity as sharp as 1 µs or less. How this perceptual feat is accomplished in the nervous system remains unresolved. Here, we examined the precision of latency registration (latency jitter) in neural population responses as a possible mechanism underlying the bat's hyperacuity. We recorded local field potentials in the cochlear nucleus and inferior colliculus of anesthetized big brown bats to sequences of sounds consisting of a simulated frequency-modulated broadcast followed, at various echo delays, by a four-echo cascade. Latencies of the first negative response peak to the broadcast and to the first echo in the cascade were shorter in the cochlear nucleus than in the inferior colliculus, but latency jitter of this peak was comparable in both brainstem nuclei. Mean latency jitter, averaged over all stimulus conditions, was 51 µs in the cochlear nucleus and 56 µs in the inferior colliculus. Latency jitter to the successive echoes in the echo cascades was larger, with means of 125 µs and 111 µs, respectively. These values are lower than values commonly reported for single-neuron latency variability in bats and other mammals, and they approach within an order of magnitude the big brown bat's psychophysical performance. Latency jitter for synchronized population responses on a scale of microseconds reduces the gap between neurophysiological and behavioral measures of acuity. Further systems-level analysis is necessary for understanding neural mechanisms of perception.NEW & NOTEWORTHY Echolocating big brown bats resolve time delays with a sharp precision of 1 µs or less. How this hyperacuity is accomplished in the auditory system is unknown. We now report that the precision of latency registration (latency jitter) in population activity from two brainstem nuclei in response to simulated echolocation sounds is in the range of tens of microseconds. These values are smaller than observed in single neuron responses and approach the bat's psychophysical acuity.