The effect of sound duration on rate–amplitude functions of inferior collicular neurons in the big brown bat, Eptesicus fuscus

Abstract

During echolocation, the amplitude and duration of echo pulses of the big brown bat, Eptesicus fuscus, covary throughout the entire course of hunting. The purpose of this study was to examine if variation in sound duration might affect the amplitude selectivity of inferior collicular (IC) neurons of this bat species under free-field stimulation conditions. A family of rate–amplitude functions of each IC neuron was obtained with different sound durations. The effect of sound duration on the neuron’s amplitude selectivity was then studied by examining the type, best amplitude, dynamic range and slope of each rate–amplitude function. The rate–amplitude functions of 83 IC neurons determined with different sound durations were either monotonic, saturated or non-monotonic. Neurons with monotonic rate–amplitude functions had the highest best amplitude, largest dynamic range but smallest slope. Neurons with non-monotonic rate–amplitude functions had the lowest best amplitude, smallest dynamic range but largest slope. The best amplitude, dynamic range and slope of neurons with saturated rate–amplitude functions were intermediate between these two types. Rate–amplitude functions of one group (47, 57%) of IC neurons changed from one type to another with sound duration and one-third of these neurons were tuned to sound duration. As a result, the best amplitude, dynamic range, and slope also varied with sound duration. However, rate–amplitude functions of the other group (36, 43%) of IC neurons were hardly affected by sound duration and two-thirds of these neurons were tuned to sound duration. Biological relevance of these findings in relation to bat echolocation is discussed.

Introduction

Sound duration is an important acoustic parameter that contributes to the distinct spectral and temporal attributes of individual biological sounds and is therefore important in animal acoustic communication and orientation (Busnel, 1967). For example, frogs use spectral and temporal cues (pulse shape, pulse repetition rate, pulse duration and pulse rise–decay times) for both communication and call discrimination (Blair, 1958, Capranica, 1966, Capranica and Moffat, 1983). Similarly, insectivorous bats such as big brown bats, Eptesicus fuscus, use long duration sounds for social communication or during cruising in the open field but use short pulses for orientation (Fenton, 1977, Griffin, 1958, Gould, 1970, Simmons et al., 1979).

To understand the importance of sound duration in acoustic signal processing, many studies have examined the duration selectivity of auditory neurons in frogs (Feng et al., 1990, Gooler and Feng, 1992), bats (Casseday et al., 1994, Casseday et al., 2000, Ehrlich et al., 1997, Galazyuk and Feng, 1997, Fuzessery and Hall, 1999, Jen and Schlegel, 1982, Jen and Feng, 1999, Jen and Zhou, 1999, Pinheiro et al., 1991, Zhou and Jen, 2001), chinchillas (Chen, 1998), mice (Brand et al., 2000) and cats (He et al., 1997). These studies demonstrated that duration-tuned auditory neurons behave as band-pass, long-pass or short-pass filters to sound duration when tested at a given sound amplitude such that they discharge maximally to a specific sound duration or a range of sound durations but the discharge drops more than 50% at other sound durations. These findings indicate that selectivity of auditory neurons to the given sound amplitude is affected by sound duration. Other studies have shown that sound duration affects the response threshold of auditory neurons and most neurons showed a lowest threshold to a specific sound duration (Galazyuk and Feng, 1997, Wu and Jen, 1995).

During hunting, big brown bats, E. fuscus, systematically increase pulse repetition rate, decrease pulse amplitude and shorten the pulse duration as they search, approach and finally intercept the insects (Griffin, 1958, Simmons et al., 1979). In this active acoustic behavior, analysis of changing echo amplitude either due to decreasing bat-to-target distance or fluttering of insects is essential for successful prey capture (Simmons et al., 1992). Because pulse amplitude and duration covary throughout the entire course of hunting, the selectivity of bat auditory neurons to one pulse parameter may conceivably be affected by the other. However, recent studies showed duration selectivity of most inferior collicular (IC) neurons is tolerant to changes in pulse amplitude (Fremouw et al., 2000, Zhou and Jen, 2001). Whether amplitude selectivity of IC neurons is also tolerant to changes in pulse duration has not been explored, although pulse duration appears to have some effect on rate–amplitude functions of IC neurons (Fuzessery, 1994, Pinheiro et al., 1991). We therefore plotted a family of rate–amplitude functions of individual IC neurons with different pulse durations that were comparable to those used by big brown bats during the search, approach and terminal phases of hunting. We then studied how different pulse durations affected the amplitude selectivity of these IC neurons by examining variation in the type, best amplitude, dynamic range and slope of rate–amplitude functions with sound duration.