Cochlear representation of wideband biosonar sounds and the emergence of neural oscillations

Abstract

Echolocating big brown bats and bottlenose dolphins broadcast wideband ultrasonic echolocation calls in the baseband to sense their surroundings. Even though these species inhabit different media and emit echolocation calls with different spectra, both show similar perceptual acuity: They determine target range from echo delay, they detect changes in echo delay on a microsecond scale, and they perceive ultrasonic phase. These perceptual performances are too acute to understand on the basis of single neuron responses, and even neural population responses do not reach the required behavioral values. Here we propose two mechanisms that may contribute to temporal hyperacuity in these wideband echolocators. Structural imaging studies show that in both species the cochlea receives input from the middle ear at locations different from that seen in non-echolocating mammals. These unusual patterns of input might produce interference patterns in traveling waves along the basilar membrane, which in turn could facilitate detection of ultrasonic phase by producing low difference frequencies that may form a substrate for further neural processing into perception. The second mechanism is related to oscillations of evoked activity observed in the bat's inferior colliculus, which could create broadcast-echo interference patterns at the neural level. The resulting difference-frequency interference signals would be very sensitive to changes in echo delay and phase. Small changes in ultrasonic sounds thus could lead to much larger changes in neural response timing by magnifying echo time itself.