Phase evaluation in hypothetical receivers simulating ranging in bats

Echo delay discrimination by the bat Eptesicus fuscus had been investigated in an experiment with simulated targets jittering in range (Simmons 1979). The dip in the resulting psychometric curve was used by Simmons to suggest the neuronal implementation of a coherent cross-correlation receiver in the auditory system of bats. By computer simulation it is shown here that the dip may be even more pronounced and less susceptible to noise with alternative receiver configurations which not necessarily evaluate signal phase information coherently, e.g., a bank of neuronal filters with envelope-processing. New behavioral experiments are suggested to critically test such model hypotheses.     

Can two streams of auditory information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus

A tenet of auditory scene analysis is that we can fully process only one stream of auditory information at a time. We tested this assumption in a gleaning bat, the pallid bat (Antrozous pallidus) because this bat uses echolocation for general orientation, and relies heavily on prey-generated sounds to detect and locate its prey. It may therefore encounter situations in which the echolocation and passive listening streams temporally overlap. Pallid bats were trained to a dual task in which they had to negotiate a wire array, using echolocation, and land on one of 15 speakers emitting a brief noise burst in order to obtain a food reward. They were forced to process both streams within a narrow 300 to 500 ms time window by having the noise burst triggered by the bats initial echolocation pulses as it approached the wire array. Relative to single task controls, echolocation and passive sound localization performance was slightly, but significantly, degraded. The bats also increased echolocation interpulse intervals during the dual task, as though attempting to reduce temporal overlap between the signals. These results suggest that the bats, like humans, have difficulty in processing more than one stream of information at a time.     

Adaptive mechanisms underlying the bat biosonar behavior

For survival, bats of the suborder Microchiropetra emit intense ultrasonic pulses and analyze the weak returning echoes to extract the direction, distance, velocity, size, and shape of the prey. Although these bats and other mammals share the common layout of the auditory pathway and sound coding mechanism, they have highly developed auditory systems to process biologically relevant pulses at the expense of a reduced visual system. During this active biosonar behavior, they progressively shorten the pulse duration, decrease the amplitude and pulse-echo gap as they search, approach and finally intercept the prey. Presumably, these changes in multiple pulse parameters throughout the entire course of hunting enable them to extract maximal information about localized prey from the returning echoes. To hunt successfully, the auditory system of these bats must be less sensitive to intense emitted pulses but highly sensitive to weak returning echoes. They also need to recognize and differentiate the echoes of their emitted pulses from echoes of pulses emitted by other conspecifics. Past studies have shown the following mechanical and neural adaptive mechanisms underlying the successful bat biosonar behavior: (1) Forward orienting and highly mobile pinnae for effective scanning, signal reception, sound pressure transformation and mobile auditory sensitivity; (2) Avoiding and detecting moving targets more successfully than stationary ones; (3) Coordinated activity of highly developed laryngeal and middle ear muscles during pulse emission and reception; (4) Mechanical and neural attenuation of intense emitted pulses to prepare for better reception of weak returning echoes; (5) Increasing pulse repetition rate to improve multiple-parametric selectivity to echoes; (6) Dynamic variation of duration selectivity and recovery cycle of auditory neurons with hunting phase for better echo analysis; (7) Maximal multiple-parametric selectivity to expected echoes returning within a time window after pulse emission; (8) Pulse-echo delaysensitive neurons in higher auditory centers for echo ranging; (9) Corticofugal modulation to improve on-going multiple-parametric signal processing and reorganize signal representation, and (10) A large area of the superior colliculus, pontine nuclei and cerebellum that is sensitive to sound for sensori-motor integration. All these adaptive mechanisms facilitate the bat to effectively extract prey features for successful hunting.     

A neural mechanism for detecting the distance of a selected target by modulating the FM sweep rate of biosonar in echolocation of bat

Most species of bats making echolocation use frequency modulated (FM) ultrasonic pulses to measure the distance to targets. These bats detect with a high accuracy the arrival time differences between emitted pulses and their echoes generated by targets. In order to clarify the neural mechanism for echolocation, we present neural model of inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC) along which information of echo delay times is processed. The bats increase the downward frequency sweep rate of emitted FM pulse as they approach the target. The functional role of this modulation of sweep rate is not yet clear. In order to investigate the role, we calculated the response properties of our models of IC, MGB, and AC changing the target distance and the sweep rate. We found based on the simulations that the distance of a target in various ranges may be encoded the most clearly into the activity pattern of delay time map network in AC, when the sweep rate of FM pulse used is coincided with the observed value which the bats adopt for each range of target distance.     

Tiger moths and the threat of bats: decision-making based on the activity of a single sensory neuron

Echolocating bats and eared moths are a model system of predator–prey interaction within an almost exclusively auditory world. Through selective pressures from aerial-hawking bats, noctuoid moths have evolved simple ears that contain one to two auditory neurons and function to detect bat echolocation calls and initiate defensive flight behaviours. Among these moths, some chemically defended and mimetic tiger moths also produce ultrasonic clicks in response to bat echolocation calls; these defensive signals are effective warning signals and may interfere with bats'' ability to process echoic information. Here, we demonstrate that the activity of a single auditory neuron (the A1 cell) provides sufficient information for the toxic dogbane tiger moth, Cycnia tenera, to decide when to initiate defensive sound production in the face of bats. Thus, despite previous suggestions to the contrary, these moths'' only other auditory neuron, the less sensitive A2 cell, is not necessary for initiating sound production. However, we found a positive linear relationship between combined A1 and A2 activity and the number of clicks the dogbane tiger moth produces.     

The role of prey-generated sounds,vision, and echolocation in prey localization by the African batCardioderma cor (Megadermatidae)

Summary Cardioderma cor responded with head movements and flight toward speakers broadcasting calls of frogs and crickets which contained only sonic frequencies. Unlike the frog-eating bat,Trachops cirrhosus, they did not make contact with the speakers. Prey movements that generated sonic and ultrasonic sounds were both sufficient and necessary for the bats to localize and capture prey. Prey dragged across a glass sheet with a thin layer of water did not generate sounds and bats did not attempt to capture these prey, even with the availability of visual and echolocation cues. There was no evidence for the use of visual cues while hunting; bats did not localize prey more readily in light than darkness. Prey were presented such that their movements initially generated sounds, but then the prey moved onto the water layer of the glass sheet and sounds were eliminated. The bats emitted echolocation signals while hunting in this situation; however, the information from these signals was not utilized. The bats landed at the site that prey last made sound. These results demonstrate the importance of passive hearing for prey localization in this bat, and further suggest that when preygenerated sounds and echolocation signals offer conflicting information the bat's behavior is guided by the former.     

Size does not matter: size-invariant echo-acoustic object classification

Echolocating bats can not only extract spatial information from the auditory analysis of their ultrasonic emissions, they can also discriminate, classify and identify the three-dimensional shape of objects reflecting their emissions. Effective object recognition requires the segregation of size and shape information. Previous studies have shown that, like in visual object recognition, bats can transfer an echo-acoustic object discrimination task to objects of different size and that they spontaneously classify scaled versions of virtual echo-acoustic objects according to trained virtual-object standards. The current study aims to bridge the gap between these previous findings using a different class of real objects and a classification—instead of a discrimination paradigm. Echolocating bats (Phyllostomus discolor) were trained to classify an object as either a sphere or an hour-glass shaped object. The bats spontaneously generalised this classification to objects of the same shape. The generalisation cannot be explained based on similarities of the power spectra or temporal structures of the echo-acoustic object images and thus require dedicated neural mechanisms dealing with size-invariant echo-acoustic object analysis. Control experiments with human listeners classifying the echo-acoustic images of the objects confirm the universal validity of auditory size invariance. The current data thus corroborate and extend previous psychophysical evidence for sonar auditory-object normalisation and suggest that the underlying auditory mechanisms following the initial neural extraction of the echo-acoustic images in echolocating bats may be very similar in bats and humans.     

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

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.     

Plant classification from bat-like echolocation signals

Classification of plants according to their echoes is an elementary component of bat behavior that plays an important role in spatial orientation and food acquisition. Vegetation echoes are, however, highly complex stochastic signals: from an acoustical point of view, a plant can be thought of as a three-dimensional array of leaves reflecting the emitted bat call. The received echo is therefore a superposition of many reflections. In this work we suggest that the classification of these echoes might not be such a troublesome routine for bats as formerly thought. We present a rather simple approach to classifying signals from a large database of plant echoes that were created by ensonifying plants with a frequency-modulated bat-like ultrasonic pulse. Our algorithm uses the spectrogram of a single echo from which it only uses features that are undoubtedly accessible to bats. We used a standard machine learning algorithm (SVM) to automatically extract suitable linear combinations of time and frequency cues from the spectrograms such that classification with high accuracy is enabled. This demonstrates that ultrasonic echoes are highly informative about the species membership of an ensonified plant, and that this information can be extracted with rather simple, biologically plausible analysis. Thus, our findings provide a new explanatory basis for the poorly understood observed abilities of bats in classifying vegetation and other complex objects.     

Echo SPL influences the ranging performance of the big brown bat,Eptesicus fuscus

Four bats of the species Eptesicus fuscus were trained in a two-alternative forced-choice procedure to discriminate between two phantom targets that differed in range. The rewarded stimulus was located at a distance of 52.7 cm, while the other unrewarded stimulus was further away. Only one target was presented at a time.In the first experiment we measured the range discrimination performance at an echo SPL of –28 dB relative to the bat's sonar transmission. A 75% correct performance level was arbitrarily defined as threshold and was obtained at a delay difference of 80 s, corresponding to a range difference of 13.8 mm.In the second experiment the delay difference was fixed at 150 s and the echo SPL varied between –8 and –48 dB relative to sonar emissions. The performance of the bats depended on the relative echo SPL. At –28 dB the bats showed the best performance. It deteriorated at an increase of the relative echo SPL to –18 dB and –8 dB. The performance also deteriorated when the relative echo SPL was reduced to –38 dB and –48 dB. Only at low relative echo SPLs did the bats partially compensate for the reduction in echo SPL and increased the SPL of their emitted signals by a few dB.Our results support the hypothesis that neurons exhibiting paradoxical latency shift may be involved in encoding target range. This hypothesis predicts a decrease in performance at high echo SPLs as we found it in our experiments. The observed reduction in performance at very low echo SPLs may be due to a decrease in S/N ratio.     

Noctuid moths show neural and behavioural responses to sounds made by some bat-marking rings

Coloured rings are often used for marking bats so that specific individuals can be recognized. We noticed that the rings of mouse-eared bats, Myotis myotis and Myotis blythii, in a combination of one plastic-split and one metallic ring on the same forearm, emitted sounds that were largely ultrasonic each time the rings met in flight. We recorded the ring sounds and the echolocation calls produced by the bats, and played them back to neural preparations of lesser yellow underwing moths, Noctua comes, while making extracellular recordings from the moths' A1 auditory receptors. The peak energy of the ring sounds occurred much closer in frequency to the moth's best auditory frequency (the frequency at which the moth has the lowest auditory threshold) than the peak energy of the calls, for both bat species, and the ring sounds were detected at a threshold 5-6 dB peSPL lower than the calls. Moths performed evasive manoeuvres to playbacks of ring sounds more frequently than they did to control (tape noise) sequences. These neural and behavioural responses imply that certain bats should not be marked with two rings on one wing, as this may make the bat more apparent to tympanate insects, and may therefore reduce its foraging success. Copyright 1999 The Association for the Study of Animal Behaviour.     

An autocorrelation model of bat sonar

Their sonar system allows echolocating bats to navigate with high skill through a complex, three- dimensional environment at high speed and low light. The auditory analysis of the echoes of their ultrasonic sounds requires a detailed comparison of the emission and echoes. Here an auditory model of bat sonar is introduced and evaluated against a set of psychophysical phantom-target, echo-acoustic experiments. The model consists of a relatively detailed simulation of auditory peripheral processing in the bat, Phyllostomus discolor, followed by a functional module consisting of a strobed, normalised, autocorrelation in each frequency channel. The model output is accumulated in a sonar image buffer. The model evaluation is based on the comparison of the image-buffer contents generated in individually simulated psychophysical trials. The model provides reasonably good predictions for both temporal and spectral behavioural sonar processing in terms of sonar delay-, roughness, and phase sensitivity and in terms of sensitivity to the temporal separations in two-front targets and the classification of spectrally divergent phantom targets.     

Acoustic imaging in bat sonar: Echolocation signals and the evolution of echolocation

Summary Echolocating bats behave as though they perceive the crosscorrelation functions between their sonar transmissions and echoes as images of targets, at least with respect to perception of target range, horizontal direction, and shape. These data imply that bats use a multi-dimensional acoustic imaging system for echolocation with broadband, usually frequencymodulated signals. The perceptual structure of the echolocation signals used by different species of bats was investigated using the crosscorrelation functions between emitted signals and returning echoes as indices of perceptual acuity.Thebandwidth andaverage period of echolocation signals are identified as the principal acoustic features of broadband sonar waveforms that determine the quality of target perceptions. The multiple-harmonic structure of echolocation sounds, which is characteristic of the broadband signals of the majority of species of bats, yields a lower average period (separation of peaks in the crosscorrelation function) than would be expected from the average frequency of the signal as a whole, sharpening target localization.The frequency-modulation of the harmonics in the sonar sounds of bats reduces the heights of side-peaks in the crosscorrelation functions of the signals, promoting sharp, unambiguous determination of target position, and leads to the well-known coupling of perception of range and velocity for moving targets. The shapes of the frequency sweeps and bandwidths of frequency modulation contribute to reducing this range-velocity coupling. Harmonic organization nearly eliminates range-velocity coupling.The use of multiple-harmonics and fairly broad frequency modulation in sonar signals yields especially sharp resolution of target position to reject clutter interference. Such signals are commonly used by bats in cluttered environments. Very broad frequency sweeps with fewer harmonics may accomplish the same effect, but the low signal periodicity contributed by harmonic structure is an important factor in banishing side-peaks in the crosscorrelation function from perception.Abbreviations ACR autocorrelation function - AMB ambiguity diagram - CF constant frequency - FM frequency modulated - LFM linear frequency sweep - LPM linear period sweep - XCR crosscorrelation function     

Thermocron iButton and iBBat temperature dataloggers emit ultrasound

Thermocron iButton dataloggers are widely used to measure thermal microclimates experienced by wild animals. The iBBat is a smaller version of the datalogger, also commercially available, that is used to measure animal skin or core body temperatures when attached externally or surgically implanted. Field observations of bats roosting under a bridge suggested that bats avoided locations with iButtons. A heterodyne bat detector revealed that the dataloggers emitted ultrasound which was detectable from a distance of up to 30 cm. We therefore recorded and quantified the acoustic properties [carrier frequency (Hz) and root mean square sound pressure level (dB SPL)] of iButton and iBBat dataloggers. All units emitted a 32.9 kHz pure tone that was readily picked up with a time expansion bat detector at a distance of 1 cm, and most were detected at a distance of 15 cm. The maximum amplitude of iButton dataloggers was 46.5 dB SPL at 1.0 cm—a level within the range of auditory sensitivity for most small mammals. Wrapping iButtons in plastic insulation severely attenuated the amplitude of ultrasound. Although there was a statistically significant reduction in rates of warming and cooling with insulation, this effect was small and we suggest that insulation may be a viable solution to eliminate unwanted ultrasonic noise in instances when small delays in thermal response dynamics are not a concern. We recommend behavioural studies to assess if the electronic signals emitted by iButtons are disturbing to small mammals.     

In vivo approach to the cellular mechanisms for sensory processing in sleep and wakefulness

1. The present review analyzes sensory processing during sleep and wakefulness from a single neuronal viewpoint. Our premises are that processing changes throughout the sleep–wakefulness cycle may be at least partially evidenced in single neurons by (a) changes in the phase locking of the response to the hippocampal theta rhythm, (b) changes in the discharge rate and firing pattern of the response to sound, and (c) changes in the effects of the neurotransmitters involved in the afferent and efferent pathways.2. The first part of our report is based on the hypothesis that the encoding of sensory information needs a timer in order to be processed and stored, and that the hippocampal theta rhythm could contribute to the temporal organization. We have demonstrated that the guinea pig's auditory and visual neuronal discharge exhibits a temporal relationship (phase locking) to the hippocampal theta waves during wakefulness and sleep phases.3. The concept that the neural network organization during sleep versus wakefulness is different and can be modulated by sensory signals and vice versa, and that the sensory input may be influenced by the CNS state, i.e., asleep or awake, is introduced. During sleep the evoked firing of auditory units increases, decreases, or remains similar to that observed during quiet wakefulness. However, there has been no auditory unit yet that stops firing as the guinea pig enters sleep. Approximately half of the cortical neurons studied did not change firing rate when passing into sleep while others increased or decreased. Thus, the system is continuously aware of the environment. We postulate that those neurons that changed their evoked firing during sleep are also related to still unknown sleep processes.4. Excitatory amino acid neurotransmitters participate in the synaptic transmission of the afferent and efferent pathways in the auditory system. In the inferior colliculus, however, the effects of glutamate's mediating the response to sound and the efferent excitation evoked by cortical stimulation failed to show differences in sleep and wakefulness.5. Considering that neonates and also infants spend most of the time asleep, the continuous arrival of sensory information to the brain during both sleep phases may serve to sculpt the brain by activity-dependent mechanisms of neural development, as has been postulated for wakefulness.     

Different Auditory Feedback Control for Echolocation and Communication in Horseshoe Bats

Auditory feedback from the animal''s own voice is essential during bat echolocation: to optimize signal detection, bats continuously adjust various call parameters in response to changing echo signals. Auditory feedback seems also necessary for controlling many bat communication calls, although it remains unclear how auditory feedback control differs in echolocation and communication. We tackled this question by analyzing echolocation and communication in greater horseshoe bats, whose echolocation pulses are dominated by a constant frequency component that matches the frequency range they hear best. To maintain echoes within this “auditory fovea”, horseshoe bats constantly adjust their echolocation call frequency depending on the frequency of the returning echo signal. This Doppler-shift compensation (DSC) behavior represents one of the most precise forms of sensory-motor feedback known. We examined the variability of echolocation pulses emitted at rest (resting frequencies, RFs) and one type of communication signal which resembles an echolocation pulse but is much shorter (short constant frequency communication calls, SCFs) and produced only during social interactions. We found that while RFs varied from day to day, corroborating earlier studies in other constant frequency bats, SCF-frequencies remained unchanged. In addition, RFs overlapped for some bats whereas SCF-frequencies were always distinctly different. This indicates that auditory feedback during echolocation changed with varying RFs but remained constant or may have been absent during emission of SCF calls for communication. This fundamentally different feedback mechanism for echolocation and communication may have enabled these bats to use SCF calls for individual recognition whereas they adjusted RF calls to accommodate the daily shifts of their auditory fovea.     

Variability of spike trains and the processing of temporal patterns of acoustic signals—problems,constraints, and solutions

Object recognition and classification by sensory pathways is rooted in spike trains provided by sensory neurons. Nervous systems had to evolve mechanisms to extract information about relevant object properties, and to separate these from spurious features. In this review, problems caused by spike train variability and counterstrategies are exemplified for the processing of acoustic signals in orthopteran insects. Due to size limitations of their nervous system we expect to find solutions that are stripped to the computational basics. A key feature of auditory systems is temporal resolution, which is likely limited by spike train variability. Basic strategies to reduce such variability are to integrate over time, or to average across several neurons. The first strategy is constrained by its possible interference with temporal resolution. Grasshoppers do not seem to explore temporal integration much, in spite of the repetitive structure of their songs, which invites for multiple looks at the signal. The benefits of averaging across neurons depend on uncorrelated responses, a factor that may be crucial for the performance and evolution of small nervous systems. In spite of spike train variability the temporal information necessary for the recognition of conspecifics is preserved to a remarkable degree in the auditory pathway.Abbreviations dB decibel - CV coefficient of variation - SNR signal to noise ratio     

Primate communication in the pure ultrasound

Few mammals-cetaceans, domestic cats and select bats and rodents-can send and receive vocal signals contained within the ultrasonic domain, or pure ultrasound (greater than 20 kHz). Here, we use the auditory brainstem response (ABR) method to demonstrate that a species of nocturnal primate, the Philippine tarsier (Tarsius syrichta), has a high-frequency limit of auditory sensitivity of ca 91 kHz. We also recorded a vocalization with a dominant frequency of 70 kHz. Such values are among the highest recorded for any terrestrial mammal, and a relatively extreme example of ultrasonic communication. For Philippine tarsiers, ultrasonic vocalizations might represent a private channel of communication that subverts detection by predators, prey and competitors, enhances energetic efficiency, or improves detection against low-frequency background noise.     

Phase sensitivity in bat sonar revisited

An echolocating bat produces echoes consisting of the convolution of echolocation call and the impulse response (IR) of the ensonified object. A crucial question in animal sonar is whether bats are able to extract this IR from the echo. The bat inner ear generates a frequency representation of call and echo and IR extraction in the frequency domain requires accurate analysis of both magnitude and phase information. Previous studies investigating the phase sensitivity of bats using a jitter paradigm reported a temporal acuity down to 10 ns, suggesting perfect sonar phase representation. In a phantom-target playback experiment, we investigate the perceptual phase sensitivity of the bat Phyllostomus discolor using a novel approach: instead of manipulating IR phase by changing IR delay (jitter paradigm), we randomized IR phase and thus lengthened the IR over time, leaving the magnitude spectrum unchanged. Our results show that phase sensitivity, as reflected in the analysis of signal duration, appears to be much lower than phase sensitivity, as reflected in the analysis of signal onset. The current data indicate that different temporal aspects of sonar processing are encoded with very different temporal resolution and thus an overall claim of “phase sensitivity” as such cannot be maintained.