Michael J. Ferragamo

Discrimination of jittered sonar echoes by the echolocating bat, Eptesicus fuscus: the shape of target images in echolocation.

Summary1.Behavioral experiments with jittering echoes examined acoustic images of sonar targets in the echolocating bat, Eptesicus fuscus, along the echo delay or target range axis. Echo phase, amplitude, bandwidth, and signal-to-noise ratio were manipulated to assess the underlying auditory processes for image formation.2.Fine delay acuity is about 10 ns. Calibration and control procedures indicate that this represents temporal acuity rather than spectral discrimination. Jitter discrimination curves change in phase when the phase of one jittering echo is shifted by 180° relative to the other, showing that echo phase is involved in delay estimation. At an echo detectability index of about 36 dB, fine acuity is 40 ns, which is approximately as predicted for the delay accuracy of an ideal receiver.3.Compound performance curves for 0° and 180° phase conditions match the crosscorrelation function of the echoes. The locations of both 0° and 180° phase peaks in the performance curves shift along the time axis by an amount that matches neural amplitude-latency trading in Eptesicus, confirming a temporal basis for jitter discrimination.

Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus.

Summary1.FM echolocating bats (Eptesicus fuscus) were trained to discriminate between a two-component complex target and a one-component simple target simulated by electronically-returned echoes in a series of experiments that explore the composition of the image of the two-component target. In Experiment I, echoes for each target were presented sequentially, and the bats had to compare a stored image of one target with that of the other. The bats made errors when the range of the simple target corresponded to the range of either glint in the complex target, indicating that some trace of the parts of one image interfered with perception of the other image. In Experiment II, echoes were presented simultaneously as well as sequentially, permitting direct masking of echoes from one target to the other. Changes in echo amplitude produced shifts in apparent range whose pattern depended upon the mode of echo presentation.2.Eptesicus perceives images of complex sonar targets that explicitly represent the location and spacing of discrete glints located at different ranges. The bat perceives the targets structure in terms of its range profile along a psychological range axis using a combination of echo delay and echo spectral representations that together resemble a spectrogram of the FM echoes. The image itself is expressed entirely along a range scale that is defined with reference to echo delay. Spectral information contributes to the image by providing estimates of the range separation of glints, but it is transformed into these estimates.3.Perceived absolute range is encoded by the timing of neural discharges and is vulnerable to shifts caused by neural amplitude-latency trading, which was estimated at 13 to 18 μs per dB from N1 and N4 auditory evoked potentials in Eptesicus. Spectral cues representing the separation of glints within the target are transformed into estimates of delay separations before being incorporated into the image. However, because they are encoded by neural frequency tuning rather than the time-of-occurrence of neural discharges, the perceived range separation of glints in images is not vulnerable to amplitudelatency shifts.4.The bat perceives an image that is displayed in the domain of time or range. The image receives no evident spectral contribution beyond what is transformed into delay estimates. Although the initial auditory representation of FM echoes is spectrogram-like, the time, frequency, and amplitude dimensions of the spectrogram appear to be compressed into an image that has only time and amplitude dimensions. The spectral information is not lost but manifests itself as equivalent time-domain information.

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).

Golgi cells in the superficial granule cell domain overlying the ventral cochlear nucleus: Morphology and electrophysiology in slices

Golgi cells are poised to integrate multimodal influences by participating in circuits involving granule cells in the cochlear nuclei. To understand their physiological role, intracellular recordings were made from anatomically identified Golgi cells in slices of the cochlear nuclei from mice. Cell bodies, dendrites, and terminals for all seven labeled cells were restricted to the narrow plane of the superficial granule cell domain over the ventral cochlear nucleus. The axonal arborization was the most striking feature of all Golgi cells; a dense plexus of terminals covered an area 200–400 μm in diameter in the vicinity of the cell body and dendrites. Axonal beads often surrounded granule cell bodies, indicating that granule cells are probable targets. Cells had input resistances up to 130 MΩ and fired regular, overshooting action potentials. Golgi cells probably receive auditory nerve input, because shocks to the cut end of the auditory nerve excited Golgi cells with excitatory postsynaptic potentials (EPSPs). The latency of EPSPs shortened to a minimum and the amplitude of EPSPs grew in several steps as the strength of shocks was increased. The minimum latency of EPSPs in Golgi cells was on average 1.3 milliseconds, 0.6 milliseconds longer than the minimum latencies of EPSPs in nearby octopus and T stellate cells. The long latency raises the possibility that Golgi cells receive input from slowly conducting, unmyelinated auditory nerve fibers. Golgi cells are also excited by interneurons with N‐methyl‐D‐aspartate receptors, probably granule cells, because repetitive shocks and single shocks in the absence of extracellular Mg2+ evoked late EPSPs that were reversibly blocked by DL‐2‐amino‐5‐phosphono‐valeric acid. J. Comp. Neurol. 400:519–528, 1998.

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.

Phase sensitivity of auditory brain‐stem responses in echolocating big brown bats

Multiple behavioral experiments show that echolocating big brown bats perceive 180° phase shifts of ultrasonic (20–100 kHz) FM echoes as delay changes of ±15 μm. These bats represent FM sweeps as coherent auditory spectrograms in which low‐pass smoothing of half‐wave‐rectified hair‐cell excitation is the critical limiting parameter. Computational modeling of auditory spectrograms combined with Monte Carlo simulation of echo delay psychophysics reveals that coherence is preserved when the auditory low‐ pass smoothing cutoff is as low as 7–10 kHz, which is not nearly as high as the 20‐ to 50‐kHz ultrasonic frequencies that seem necessary intuitively. Local‐field‐potential recordings from the bat’s auditory brain‐stem are sensitive to the starting phase of tone‐bursts at frequencies up to 14 kHz, manifested as a change in LFP wave‐form shape with phase. For most sites this phase sensitivity exhibits a strong dependence on stimulus amplitude. Typically, tone‐bursts of 65–75 dB SPL evoke significant changes in...

Coding of phase structure in complex sounds by bullfrog auditory‐nerve fibers

This experiment explored how the peripheral coding of the spectral and temporal structure of a complex communication signal is affected by the phase relations between individual frequency components in the sound. Complex sounds with 21 components, all of which were harmonics of a common, low‐frequency fundamental (100 Hz), were digitally synthesized. The frequencies and amplitudes of the individual components matched those of the bullfrogs species‐specific advertisement call. For one stimulus, the 21 components were generated in cosine phase, and for the other stimulus, the 21 components were in random phase. Most amphibian papilla (AP) and basilar papilla (BP) fibers synchronized to the envelope only of the phase‐coherent stimulus, and the complex spectral structure of the stimulus was not accurately encoded by population firing patterns. Envelope synchronization to the random‐phase stimulus was not seen in the responses of some mid‐frequency‐sensitive AP and BP fibers, although low‐frequency‐sensitive ...