Tim Haresign

Spatially dependent acoustic cues generated by the external ear of the big brown bat, Eptesicus fuscus

To measure the directionality of the external ear of the echolocating bat, Eptesicus fuscus, the left or right eardrum of a dead bat was replaced by a microphone which recorded signals received from a sound source that was moved around the stationary head. The test signal was a 0.5-ms FM sweep from 100 kHz to 10 kHz (covering all frequencies in the bats biosonar sounds). Notches and peaks in transfer functions for 7 tested ears varied systematically with changes in elevation. For the most prominent notch, center frequency decreased from about 50 kHz for elevations at or near the horizontal to 30-40 kHz for elevations 30 degrees-40 degrees below the horizontal. A second notch shifted from about 85 kHz to 70 kHz over these same elevations. Above the horizontal, a peak that flanks these notches changed in amplitude by 15 dB with changes in elevation. Removal of the tragus from the external ear disrupted the systematic movement of notch frequencies with elevation but did not disrupt changes in the peaks amplitude. Smaller changes in notch frequency also occurred with changes in azimuth, so monaural notch information alone cannot determine the position of sound sources away from the median plane. However, because bats routinely keep the head pointed at the targets azimuth, median-plane localization occurs with monaural cues delivered to the two ears. Corresponding changes with elevation occurred in the impulse-response, which consists of a series of 3-6 peaks spaced 10-20 microseconds apart. The time separation of two prominent impulse peaks systematically increased from 22-26 microseconds above the horizontal to about 36-40 microseconds below the horizontal, and removal of the tragus disrupted this time shift below the horizontal.

Auditory Dimensions of Acoustic Images in Echolocation

Echolocation in bats is one of the most demanding adaptations of hearing to be found in any animal. Transforming the information carried by sounds into perceptual images depicting the location and identity of objects rapidly enough to control the decisions and reactions of a swiftly flying bat is a prodigious task for the auditory system to accomplish. The exaggeration of aspects of auditory function to achieve spatial imaging reflects the vital role of hearing in the lives of bats — for finding prey and perceiving obstacles to flight (Neuweiler 1990). It also highlights the mechanisms behind these functions to make echolocation a useful model for studying how the auditory system processes information and creates auditory perceptions in the most extreme circumstances.

Composition of biosonar images for target recognition by echolocating bats

Abstract Echolocating bats can recognize flying insects as sonar targets in a variety of different acoustic situations ranging from open spaces to dense clutter. Target classification must depend on perceiving images whose dimensions can tolerate intrusion of additional echoes from other objects, even echoes arriving at about the same time as those from the insect, without disrupting image organization. The big brown bat, Eptesicus fuscus, broadcasts FM sonar sounds in the 15–100 kHz band and perceives the arrival-time of echoes with an accuracy of 10–15 ns and a two-point resolution of 2 μs, which suggests that perception of fine detail on the dimension of echo delay or target range is the basis for reconstructing complex acoustic scenes and recognizing targets that are embedded in these scenes. The directionality of the bats sonar sound is very broad, making it impossible to isolate echoes from individual targets merely by aiming the head and ears at one object instead of another. Consequently, segregation of targets must depend on isolating their echoes as discrete events along the axis of delay. That is, the bats images must correspond to impulse responses of target scenes. However, the bats sonar broadcasts are several milliseconds long, and the integration time of echo reception is about 350 μs, so perception of separate delays for multiple echoes only a few microseconds apart requires deconvolution of spectrally-complex echoes that overlap and interfere with each other within the 350-μs integration time. The bats auditory system encodes the FM sweeps of transmissions and echoes as half-wave-rectified, magnitude-unsquared spectrograms, and then registers the time that elapses between each frequency in the broadcast and the echo, effectively correlating the spectrograms. The interference patterns generated by overlap of multiple echoes are then used to modify these delay estimates by adding fine details of the delay structure of echoes. This is equivalent to transformation of the spectrograms into the time domain, or deconvolution of echo spectra by spectrogram correlation and transformation (SCAT). However, while deconvolution overcomes integration time, the bats receiving antennas reverberate for about 100 μs, smearing the echoes upon arrival. The bat overcomes this problem by receiving echoes from different directions than the transmitted sound, which radiates from the mouth. The broad range of antenna reverberations common to the emission and echoes thus cancel out, leaving only narrow elevation-dependent differences, which in fact appear in the bats images. The SCAT algorithms successfully recreate images comparable to those perceived by the bat and provide for classification of targets from their glint structure in different situations.

Frequency tuning, latencies, and responses to frequency-modulated sweeps in the inferior colliculus of the echolocating bat, Eptesicus fuscus

Abstract Neurons in the inferior colliculus (IC) of the awake big brown bat, Eptesicus fuscus, were examined for joint frequency and latency response properties which could register the timing of the bats frequency-modulated (FM) biosonar echoes. Best frequencies (BFs) range from 10 kHz to 100 kHz with 50% tuning widths mostly from 1 kHz to 8 kHz. Neurons respond with one discharge per 2-ms tone burst or FM stimulus at a characteristic latency in the range of 3–45 ms, with latency variability (SD) of 50 μs to 4–6 ms or more. BF distribution is related to biosonar signal structure. As observed previously, on a linear frequency scale BFs appear biased to lower frequencies, with 20–40 kHz overrepresented. However, on a hyperbolic frequency (linear period) scale BFs appear more uniformly distributed, with little overrepresentation. The cumulative proportion of BFs in FM1 and FM2 bands reconstructs a scaled version of the spectrogram of FM broadcasts. Correcting FM latencies for absolute BF latencies and BF time-in-sweep reveals a subset of IC cells which respond dynamically to the timing of their BFs in FM sweeps. Behaviorally, Eptesicus perceives echo delay and phase with microsecond or even submicrosecond accuracy and resolution, but even with use of phase-locked FM and tone-burst stimuli the cell-by-cell precision of IC time-frequency registration seems inadequate by itself to account for the temporal acuity exhibited by the bat.

Auditory Computations for Biosonar Target Imaging in Bats

Bats are nocturnal flying mammals classified in the order Chiroptera. These animals have evolved a biological sonar, called echolocation, to orient in darkness—to guide their flight around obstacles and to detect their prey (Griffin 1958; Novick 1977; Neuweiler 1990; see Popper and Fay 1995). Echolocating bats broadcast ultrasonic sonar signals that travel outward into the environment, reflect or scatter off objects, and return to the bat’s ears as echoes. First the outgoing sonar signal and then the echoes impinge on the ears to act as stimuli, and the bat’s auditory system processes the information carried by these sounds to reconstruct images of targets (Schnitzler and Henson 1980; Simmons and Kick 1984; Suga 1988, 1990; Simmons 1989; Dear, Simmons, and Fritz 1993; Dear et al. 1993).

Representation of Perceptual Dimensions of Insect Prey During Terminal Pursuit by Echolocating Bats

The echolocating big brown bat, Eptesicus fuscus, broadcasts brief frequency-modulated (FM) ultrasonic sounds and perceives objects from echoes of these sounds returning to its ears. Eptesicus is an insectivorous species that uses sonar to locate and track flying prey. Although the bat normally hunts in open areas, it nevertheless is capable of chasing insects into cluttered environments such as vegetation, where it completes interceptions in much the same manner as in the open except that it has to avoid the obstacles as well as catch the insect. During pursuit, the bat shortens its sonar signals and increases their rate of emission as it closes in to seize the target, and it keeps its head pointed at the insect throughout the maneuver. In the terminal stage of interception, the bat makes rapid adjustments in its flight-path and body posture to capture the insect, and these reactions occur whether the bat is pursuing its prey in the open or close to obstacles such as vegetation. Insects can be distinguished from other objects by the spectrum and phase of their echoes, and Eptesicus is very good at discriminating these acoustic features. To identify the insect in the open, but especially to distinguish which object is the insect in clutter, the bat must have some means for representing these features throughout the interception maneuver. Moreover, continuity for perception of these features is necessary to keep track of the prey in complex surroundings, so the nature of the auditory representations for the spectrum and phase of echoes has to be conserved across the approach, tracking, and terminal stages. The first problem is that representation of changes in the phase of echoes requires neural responses in the bats auditory system to have temporal precision in the microsecond range, which seems implausible from conventional single-unit studies in the bats inferior colliculus, where the temporal jitter of responses typically is hundreds of microseconds. Another problem is that echoes do not explicitly evoke neural responses in the inferior colliculus distinct from responses evoked by the broadcast during the terminal stage because the delay of echoes is too short for responsiveness to recover from the emissions. In contrast, each emission and each echo evokes its own responses during the approach and tracking stages of pursuit. How does the bat consistently represent the phase of echoes in spite of these evident limitations in neural responses? Local multiunit responses recorded from the inferior colliculus of Eptesicus reveal a novel format for encoding the phase of echoes at all stages of interception. Changes in echo phase (0 degree or 180 degrees) produce shifts in the latency of responses to the emission by hundreds of microseconds, an unexpected finding that demonstrates the existence of expanded time scales in neural responses representing the target at all stages of pursuit.

Dynamic Mechanisms of Perception Exhibited by Bat Biosonar

Understanding the nature of the physiological processes that underlie perception means knowing the identity of the neuronal events whose occurrence causes a particular percept to happen. The most widely-accepted explanation for perception presently is based on analysis of stimuli into sets of parallel features, and the visual system is the sense from which most of the evidence is drawn. Individual neurons are observed to be sensitive to a specific range along one or more stimulus dimensions (the “receptive field”), and the stimulus as a whole is thought to be encoded by the inventory of features implicit in the collective activity of populations of neurons having different, but overlapping, selectivities. The response-rate or strength of the response in each neuron is the basis for feature coding; the content of the perceived image is derived from the profile of response strengths across these neuronal populations as a kind of “rate-place” image in the brain. The feature-inventory model assigns the timing of responses a vital role in grouping features into perceptual wholes (binding; see Singer, 1996; von der Malsburg, 1996), but it still leaves the content of the image along each feature dimension to be determined by the strength of the response, or response-rate in each neuron. In some perceptual systems, though, the timing of neural responses plays a role in defining the content of the image, at least at peripheral stages of neural processing (Carr, 1993; Heiligenberg, 1991; Konishi et al., 1988; O’Neill, 1995; Simmons et al., 1996; Suga et al., 1995). Most current evidence from these systems suggests that at least part of the information carried by the timing of responses at more peripheral locations is re-coded as feature information by coincidence-detecting neuronal circuits (see Hopfield, 1995).

Wavelet‐like transforms in the auditory system of the bat

Traditional views of neural processing of auditory signals in the nervous system have been shaped by conceptual models based on Fourier analysis—in the frequency domain for spectral selectivity or in the time domain for periodicity analysis. However, in recent years wavelet analysis has been proven to be a powerful new technique for signal processing. Evidence has been found for a wavelet‐like representation of ultrasonic auditory signals in the inferior colliculus of the big brown bat, Eptesicus fuscus. The inferior colliculus is a laminar structure, with the neurons in each layer being sensitive to a specific, narrow frequency band. In response to a broadband stimulus the averaged activity of small groups of neurons exhibits a structured temporal pattern in its response. The temporal response pattern is dependent on the spectral‐temporal structure of the input sound, and varies as a function of the frequency lamina from which the measurements are taken. Based on these results, it seems likely that infor...

Results of tonotopic and echo delay‐tuning mapping of the auditory cortex of the Big Brown Bat

Characterization of the response properties of neurons in the auditory cortex of Eptesicus fuscus is an initial step toward defining the neural mechanisms that mediate echolocation in FM emitting bats. Multiple‐ and single‐unit recordings from the cortex were obtained during multiple presentation of pure tones, FM sweeps, and FM sweeps in pulse‐echo pairs decreasing in delay from 40 to 0 ms. The existence of a distribution of high to low frequencies from the anterior to posterior poles of auditory cortex suggests a tonotopic map. The frequencies comprising the first harmonic of the echolocation emission appear to be magnified in their cortical representation. Frequency tuning and onset latencies in response to FM sweeps with a 20‐kHz bandwidth are similar to responses to pure tones. While the majority of cells sampled are not echo delay tuned, delay‐tuned cells have been found with best delays ranging from approximately 3–30 ms. These neurons cluster into two distinct groups suggesting regions of function...