The adaptive value of increasing pulse repetition rate during hunting by echolocating bats

doi:10.1007/s11515-012-1212-4

Front Biol

2013, Vol. 8

Issue (2) : 198-215 https://doi.org/10.1007/s11515-012-1212-4

REVIEW

The adaptive value of increasing pulse repetition rate during hunting by echolocating bats

Philip H.-S. JEN(

)

Division of Biological Sciences, University of Missouri, Columbia, MO 65211, USA

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Abstract

During hunting, bats of suborder Microchiropetra emit intense ultrasonic pulses and analyze the weak returning echoes with their highly developed auditory system to extract the information about insects or obstacles. These bats progressively shorten the duration, lower the frequency, decrease the intensity and increase the repetition rate of emitted pulses as they search, approach, and finally intercept insects or negotiate obstacles. This dynamic variation in multiple parameters of emitted pulses predicts that analysis of an echo parameter by the bat would be inevitably affected by other co-varying echo parameters. The progressive increase in the pulse repetition rate throughout the entire course of hunting would presumably enable the bat to extract maximal information from the increasing number of echoes about the rapid changes in the target or obstacle position for successful hunting. However, the increase in pulse repetition rate may make it difficult to produce intense short pulse at high repetition rate at the end of long-held breath. The increase in pulse repetition rate may also make it difficult to produce high frequency pulse due to the inability of the bat laryngeal muscles to reach its full extent of each contraction and relaxation cycle at a high repetition rate. In addition, the increase in pulse repetition rate increases the minimum threshold (i.e. decrease auditory sensitivity) and the response latency of auditory neurons. In spite of these seemingly physiological disadvantages in pulse emission and auditory sensitivity, these bats do progressively increase pulse repetition rate throughout a target approaching sequence. Then, what is the adaptive value of increasing pulse repetition rate during echolocation? What are the underlying mechanisms for obtaining maximal information about the target features during increasing pulse repetition rate? This article reviews the electrophysiological studies of the effect of pulse repetition rate on multiple-parametric selectivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus using single repetitive sound pulses and temporally patterned trains of sound pulses. These studies show that increasing pulse repetition rate improves multiple-parametric selectivity of inferior collicular neurons. Conceivably, this improvement of multiple-parametric selectivity of collicular neurons with increasing pulse repetition rate may serve as the underlying mechanisms for obtaining maximal information about the prey features for successful hunting by bats.

Keywords bat echolocation inferior colliculus multiple-parametric selectivity pulse repetition rate

Corresponding Author(s): JEN Philip H.-S.,Email:jenp@missouri.edu

Issue Date: 01 April 2013

Cite this article:

Philip H.-S. JEN. The adaptive value of increasing pulse repetition rate during hunting by echolocating bats[J]. Front Biol, 2013, 8(2): 198-215.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-1212-4
https://academic.hep.com.cn/fib/EN/Y2013/V8/I2/198

Fig.1 A: Rate-intensity functions of one monotonic (Ab) and two non-monotonic (Aa, Ac) inferior collicular neurons showing variation in the number of impulses with stimulus intensity. B: Latency-intensity functions of three inferior collicular neurons showing variation in latency (ms) with stimulus intensity ().

Fig.2 A, B: The latency-pulse repetition rate (PRR) curves of inferior collicular neurons showing the variation of latency with PRR. The latency of one type of collicular neurons increased with PRR (A1a, b) and that of the second type either hardly changed (B1b) or fluctuated within 3 ms (B1a) with PRR. The mean latency shift at each PRR for these two types of collicular neurons are shown in A2 and B2. The vertical bar at each point represents one standard deviation. The number () of data points averaged at each PRR (pps) is shown at the far right of each panel. significance level from one-way ANOVA ().

Fig.3 A, B: The minimum threshold-PRR curves of inferior collicular neurons showing the variation of minimum threshold with PRR. The minimum threshold of one type of collicular neurons increased with PRR (A1a, b) and that of the second type fluctuated within 5 dB (B1a, b) with PRR. The mean minimum threshold variation at each PRR for these two types of neurons is shown in A2 and B2. (see Fig. 1 for legends, from ).

Fig.4 Three 300 ms temporally patterned trains of sound pulses at different PRRs used to study the multiple-parametric selectivity of inferior collicular neurons. The number of pulses is shown within each pulse train. The pulse duration (PD) inter-pulse gap (IPG), inter-pulse interval (IPI) and pulse repetition rate (PRR) are shown at the bottom of the three pulse trains.

Fig.5 A: Peri-stimulus-time (PST) histograms showing the discharge pattern of a collicular obtained with 300 ms pulse trains containing 9 sound pulses of 4 ms before (Aa) and during (Ab) bicuculline application. The position of sequentially presented pulses is shown at the bottom and the neuron’s number of impulses in response to 32 presentations of each pulse is shown within each PST histogram. B: The average number of impulses discharged to sequentially presented sound pulses before (unfilled circles) and during (filled circles) bicuculline application. Bicuculline application produced significant increase in the number of impulses in response to each sound pulse (filled circles vs. unfilled circles, paired t-test, ***<0.001 and **<0.01). Note that the average number of impulses significantly decreased with sequentially presented sound pulses only before (unfilled circles) but not during (filled circles) bicuculline application (one-way ANOVA, <0.0001 vs.>0.05). C: The average percent increase in the number of impulses in response to each sound pulse during bicuculline application. Note that the percent change progressively increased with sequentially presented sound pulses (one-way ANOVA, <0.0001). The , , and represent the number of collicular neurons studied, correlation coefficient, slope and significance level for each linear regression line ().

Fig.6 A: PST histograms showing the discharge pattern of a collicular neuron obtained with 300 ms pulse trains before (Aa) and during (Ab) GABA application. B: The average number of impulses discharged to sequentially presented sound pulses before (unfilled circles) and during (filled circles) GABA application. GABA application significant decreased the number of impulses elicited by each sound pulse (filled circles vs. unfilled circles, paired t-test, ***<0.001, **<0.01 and *<0.05). Note that the average number of impulses significantly decreased with sequentially presented sound pulses only before (unfilled circles) but not during (filled circles) GABA application (one-way ANOVA, <0.0001 vs.>0.05). C: The average percent decrease in the number of impulses elicited by each sound pulse during GABA application. Note that the percent change in the number of impulses progressively decreased with sequentially presented sound pulses (one-way ANOVA, <0.0001 (Fig. 5 for legends, from ).

Fig.7 A-D: Directional selectivity curves of four collicular neurons plotted with the number of impulses obtained with three temporally patterned pulse trains of different PRRs (i.e. Fig. 4). Each horizontal dashed line indicates the 50% maximal response. Directional selectivity curves of two neurons (A,B) were not affected by the PRR while that of other two neurons (C,D) changed from one type to another. Note that the best azimuth of one neuron moved toward the midline as the PRR of the pulse train increased from 10 pps to 30 pps (B arrow). E, F: Distribution of the best azimuth of individual collicular neurons determined with pulse trains of different PRRs. The best azimuths of most collicular neurons were not affected by PRR of the pulse train (shown as filled circles within unfilled circles, or filled triangles within unfilled circles). However, best azimuths of 16%-21% neurons shifted with increasing PRR of the pulse train (filled and unfilled arrows). The best azimuth of all but one neuron shifted toward the midline with increasing PRR of the pulse trains (filled arrows in A, B) (from Zhou and Jen, 2002).

Fig.8 A, B: Directional sensitivity curves of two collicular neurons plotted with three temporally patterned pulse trains of different PRRs before and during bicuculline application. The nAR determined before and during bicuculline application and the percentage change (%?) of nAR are shown within each plot. Note that the directional selectivity curve of neuron A changed from directional to non-directional during bicuculline application so that the nAR is not available during drug application (see text for details, from Zhou and Jen, 2002).

Fig.9 A, B, C: The threshold-frequency tuning curve (FTC) of a collicular neuron measured with three temporally patterned pulse trains of different PRRs before (A-1, B-1, C-1) and during (A-2,B-2,C-2) bicuculline application. The sharpness of each FTC was expressed by Q values. D, E, F: Isolevel-FTC of a collicular neuron measured with three pulse trainsat three PRRs before (D-1, E-1,F-1) and during (D-2, E-2, F-2) bicuculline application. The sharpness of each FTC was expressed by the bandwidths at 90, 75 and 50% of maximal response (from ).

Fig.10 Rate-intensity functions of two collicular neurons determined with three temporally patterned pulse trains of different PRRs. The dynamic range (DR) of each rate-intensity function was the intensity range corresponding to the number of impulses that was 10% below the maximum and 10% above the minimum (A1, indicated by dotted lines). The slope (%/dB) of the rate-intensity function was obtained by dividing the percent change in the number of impulses within the DR by the DR (from ).

Fig.11 Duration tuning curves of four collicular neurons. Left and right ordinates represent the number of impulses per 32 presentations of pulse trains and normalized response. The abscissa represents pulse duration (ms). Duration tuning properties of these neurons are (A) band-pass, (B) short-pass, (C) long-pass and (D) all-pass. Each horizontal dashed line indicates the 50% maximal response. Duration selectivity of each curve is expressed with a best duration (BD) and a normalized duration width (nDW). The BD (ms) of the band-, short- and long-pass duration tuning curves is indicated with an arrow. An nDW (impulses/ ms) is obtained by dividing the maximum by the duration width (DW indicated with a double arrow-headed bar) of a duration tuning curve at 75% maximum (from Wu and Jen, 2006).

Fig.12 A, B, C: Peri-stimulus-time (PST) histograms showing the discharge patterns of a collicular neuron obtained with three temporally patterned pulse trains containing pulses of different durations (shown at far right) before (predrug) and during bicuculline application. D,E,F: The neuron’s duration tuning curves plotted with the total number of impulses (shown at the right of each histogram) before (unfilled circles) and during (filled circles) bicuculline application. The type, BD (ms) and nDW (impulses/ms) of the duration tuning curve are shown within each plot. NA indicates that a BD is not available (from Wu and Jen, 2006).

Fig.13 A, B, C: Peri-stimulus-time (PST) histograms showing the discharge patterns of a collicular neuron obtained with three temporally patterned pulse trains containing pulses of different durations (shown at far right) before (predrug) and during bicuculline application. D,E,F: The neuron’s duration tuning curves obtained before (unfilled circles) and during (filled circles) GABA application (Fig. 12 for legends, from Wu and Jen, 2006).

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