FM Sweep Research Articles

Application of the oddball paradigm for investigating predictive coding in the bat auditory system

Predictive coding is a theoretical framework for explaining how the auditory system efficiently codes the auditory scene by focusing on unexpected deviations. It is hypothesized that predictive coding plays a prominent role in the auditory processing of biosonar echo streams. At least two complementary biological mechanisms contribute to predictive coding: stimulus-specific adaptation (SSA), a reduced response to repetitive stimuli that emerges early in the ascending auditory pathway, and mismatch negativity (MMN), an enhanced response to low-probability stimuli mediated by the descending cortical feedback. Here, we utilized the oddball paradigm, an experimental design that measures the brain’s sensitivity to rare (deviant) stimuli, to detect and measure SSA and MMN in the auditory brainstem response (ABR) of anesthetized free-tailed bats. We predicted that SSA would be detectable in the early ABR peaks, and that MMN, if present, should appear in the slower P0 waves reflecting cortical influences on auditory expectations. Stimuli consisted of paired tones, FM sweeps, and other naturalistic stimuli, and we tested the effects of varying stimulus probabilities from 50/50 to 90/10. Results show that both SSA and MMN were detectable and separable even in early peaks of the ABR waveform.

Cognitive perception of biosonar echo delay, phase, and spectrum

FM echolocating big brown bats combine the acoustic delay, phase, and spectrum of echoes into a unitary cognitive attribute of perceived delay. In this talk, we will present psychophysical, neurophysiological, and modeling data showing how this might be accomplished. Delay accuracy measured psychophysically approximates coherent matched-filter accuracy. Psychophysical curves of echo-delay resemble pulse-echo crosscorrelation functions, with phase manifested directly within 20 μs. Computational modeling shows that low-pass time-frequency bandpass filtering at 10 kHz enables the contribution from phase. Neural responses from the auditory midbrain are phase-sensitive for tone-burst offsets up to15 kHz. Echo spectrum (spectral nulls and ripples) is transformed into psychophysical percepts of delay. The external-ear spectral null creates an elevation-dependent peak at about 35 μs for vertical target tracking. Off-axis clutter masking is suppressed by a Gestalt-like normalization process that operates within delay percepts. The organization of perceived delay and the appearance of phase shifts is facilitated by delay processing that begins at the low-frequency tail end of FM sweeps and the linking of 1st and 2nd harmonic frequencies. Surprisingly, this result requires the entire echo to be received before any delay is determined. The implications of this result will be discussed. [Work supported by ONR.]

Oscillatory discharges in the auditory midbrain of the big brown bat contribute to coding of echo delay.

Subsequent to his breakthrough discovery of delay-tuned neurons in the bat's auditory midbrain and cortex, Albert Feng proposed that neural computations for echo delay involve intrinsic oscillatory discharges generated in the inferior colliculus (IC). To explore further the presence of these neural oscillations, we recorded multiple unit activity with a novel annular low impedance electrode from the IC of anesthetized big brown bats and Seba's short-tailed fruit bats. In both species, responses to tones, noise bursts, and FM sweeps contain long latency components, extending up to 60ms post-stimulus onset, organized in periodic, oscillatory-like patterns at frequencies of 360-740Hz. Latencies of this oscillatory activity resemble the wide distributions of single neuron response latencies in the IC. In big brown bats, oscillations lasting up to 30ms after pulse onset emerge in response to single FM pulse-echo pairs, at particular pulse-echo delays. Oscillatory responses to pulses and evoked responses to echoes overlap extensively at short echo delays (5-7ms), creating interference-like patterns. At longer echo delays, responses are separately evident to both pulses and echoes, with less overlap. These results extend Feng's reports of IC oscillations, and point to different processing mechanisms underlying perception of short vs long echo delays.

Deficits in Acoustic Startle Reactivity and Auditory Temporal Processing after Traumatic Brain Injury.

Traumatic brain injury (TBI) exacts significant neurological and financial costs on patients and their families. In adult patients with moderate-to-severe TBI, central auditory impairments have been reported. These auditory impairments may interfere with language receptivity, as observed in children with developmental brain injury. Although rodent models of TBI have been widely used to examine behavioral outcomes, few studies have evaluated how TBI affects higher-order central auditory processing across a range of cue complexities. Here, auditory processing was assessed using a modified acoustic startle paradigm. We used a battery of progressively complex stimuli (single-tone, silent gaps in white noise, and frequency-modulated [FM] sweeps) in adult rats that received unilateral controlled cortical impact injury. TBI subjects showed significant reductions in acoustic startle absolute responses across nearly all stimuli, regardless of cue, duration of stimuli, or cue complexity. Despite this overall reduction of startle magnitudes in injured animals, the detection of single-tone stimuli was comparable between TBI and sham-injured subjects, indicating intact hearing after TBI. TBI subjects showed deficits in rapid gap (5 ms) and FM sweep (175 ms) detection, and, in contrast to shams, they did not improve on detecting silent gaps and FM sweeps across days of testing. Our findings provide evidence for both low-level (brainstem-mediated) and higher-order central auditory processing deficits in a rodent model of TBI, which parallel sensory impairments observed in TBI patients. The present findings support the use of modified pre-pule auditory detection paradigms to investigate clinically relevant processes in TBI.

Topographical distribution of spectrotemporal receptive field properties in the bat primary auditory cortex

Spectrotemporal modulations are a prominent feature of natural sounds including animal vocalizations and human speech. Echolocating bats must process spectrotemporal cues such as echo delays and spectrum properties to navigate their environment; however, the neuronal networks in the primary auditory cortex (A1) that process features of natural sounds remain incompletely understood. Here, we investigated the topographical distribution of tuning properties throughout A1 of Mexican free-tailed bats. While the majority of the bats’ A1 neurons are tuned to downward FM sweeps, the entire cortex is required to capture and categorize patterns of spectral details embedded within each biosonar echo. We captured the neural responses of the A1 to complex acoustic stimuli using linear, 16-channel translaminar microelectrode arrays. We analyzed 145 spectrotemporal receptive fields (STRFs) across A1, as well as the spectral and temporal modulation transfer functions (sMTF and tMTF, respectively) to determine neural tuning preferences in the spectral and temporal dimensions. We found evidence of neuronal sub-categories that were classified as having simple or complex (multi-peaked) STRFs. For simple STRFs, sMTFs and tMTFs were evaluated as a function of best frequency, and spatial location and revealed tonotopic trends similar to those reported for non-specialized animals.

Functional organization of the primary auditory cortex of the free-tailed bat Tadarida brasiliensis.

The Mexican free-tailed bat, Tadarida brasiliensis, is a fast-flying bat that hunts by biosonar at high altitudes in open space. The auditory periphery and ascending auditory pathways have been described in great detail for this species, but nothing is yet known about its auditory cortex. Here we describe the topographical organization of response properties in the primary auditory cortex (AC) of the Mexican free-tailed bat with emphasis on the sensitivity for FM sweeps and echo-delay tuning. Responses of 716 units to pure tones and of 373 units to FM sweeps and FM-FM pairs were recorded extracellularly using multielectrode arrays in anesthetized bats. A general tonotopy was confirmed with low frequencies represented caudally and high frequencies represented rostrally. Characteristic frequencies (CF) ranged from 15 to 70kHz, and fifty percent of CFs fell between 20 and 30kHz, reflecting a hyper-representation of a bandwidth corresponding to search-phase echolocation pulses. Most units showed a stronger response to downward rather than upward FM sweeps and forty percent of the neurons interspersed throughout AC (150/371) showed echo-delay sensitivity to FM-FM pairs. Overall, the results illustrate that the free-tailed bat auditory cortex is organized similarly to that of other FM-type insectivorous bats.

Laminar Organization of FM Direction Selectivity in the Primary Auditory Cortex of the Free-Tailed Bat.

We studied the columnar and layer-specific response properties of neurons in the primary auditory cortex (A1) of six (four females, two males) anesthetized free-tailed bats, Tadarida brasiliensis, in response to pure tones and down and upward frequency modulated (FM; 50 kHz bandwidth) sweeps. In addition, we calculated current source density (CSD) to test whether lateral intracortical projections facilitate neuronal activation in response to FM echoes containing spectrally distant frequencies from the excitatory frequency response area (FRA). Auditory responses to a set of stimuli changing in frequency and level were recorded along 64 penetrations in the left A1 of six free-tailed bats. FRA shapes were consistent across the cortical depth within a column and there were no obvious differences in tuning properties. Generally, response latencies were shorter (<10 ms) for cortical depths between 500 and 600 μm, which might correspond to thalamocortical input layers IIIb–IV. Most units showed a stronger response to downward FM sweeps, and direction selectivity did not vary across cortical depth. CSD profiles calculated in response to the CF showed a current sink located at depths between 500 and 600 μm. Frequencies lower than the frequency range eliciting a spike response failed to evoke any visible current sink. Frequencies higher than the frequency range producing a spike response evoked layer IV sinks at longer latencies that increased with spectral distance. These data support the hypothesis that a progressive downward relay of spectral information spreads along the tonotopic axis of A1 via lateral connections, contributing to the neural processing of FM down sweeps used in biosonar.

Bio-inspired generalizable-focusing wideband FM sonar

The bat’s inner ear and auditory brainstem register successive frequencies in FM sweeps of broadcasts and echoes with single spikes. Using the neural spectrogram of each broadcast as reference, spike latencies trace the FM sweeps for imaging echo delay by spectrogram correlation. If mutually-interfering glint reflections are present, the echo’s neural spectrogram has regularly-spaced ripples caused by amplitude-latency trading. Glint-delay estimates are generated by transforming the ripple pattern from frequency to time in real time using feedforward inhibition. Several glint delay estimates can coexist in focused target images before accumulation of nulls generates too many glint estimates and blurs the image. Echo lowpass filtering, characteristic of clutter, affects a wide swath of frequencies and changes the slope of the neural spectrogram, which evokes multiple nulls and causes image blurring that suppresses the clutter. Echo Doppler shifts also change the slope of the FM sweep, and the same mechanism is capable of blurring Doppler-shifted images so that troublesome ambiguity is suppressed. By internally adjusting the neural FM sweep of the broadcast reference, the images of echoes can be refocused onto any desired location not only in range, azimuth, and elevation, but also on the range-Doppler plane. [Work supported by ONR.]

Comparison between sub-ms fast spatio-temporal imaging and electrical recordings from the bat inferior colliculus using a micro-endoscope

Recently, we demonstrated that our micro-endoscopic system enabled acquiring optical image in submillisecond temporal resolution (132 μs/line) by line-scan. The micro-endoscope was fabricated from optical fiber bundle as an endoscope tip and the bundle was coated by gold and enamel. The tip was beveled as cone-shape for minimal invasion and the surrounding edge became electrical-conductive for being used as an electrode. Then, this system can record electrical activities (local field potentials; LFP, and multi-unit activities; MUA) at a sampling rate of 20 kHz and optical responses (calcium response derived from Oregon green BAPTA-1, AM; ΔF/F) simultaneously. We recorded these responses from the inferior colliculus (IC) of two species of bats (Carollia perspicillata and Eptesicus fuscus) to tone bursts (10, 20, 40, 60, and 80 kHz), noise bursts (5-100 kHz), and downward FM sweeps (80-20 and 100-30 kHz). Along the same scanning line, several activated areas (hot spots) were found responding to a single sou...

Functional optical imaging from bat inferior colliculus using a micro-endoscope

We developed a confocal micro-endoscopic system that enables simultaneous recording of electrical neuronal responses—local field potentials (LFPs) and multi-unit activities, (MUA) — and fluorescence changes reflecting calcium activation derived from Oregon green dye. We recorded these responses from different depths of the inferior colliculus (IC) in two species of bats (Carollia perspicillata and Eptesicus fuscus) to tone bursts, noise bursts, and FM sweeps. Electrical responses were fast and registered the occurrence of sounds with submillisecond and millisecond precision. LFPs contained strong onset responses and weaker, extended oscillations that persisted for much of the sound’s duration. In contrast, calcium responses were slow, building up gradually over the course of 50-100 ms, and declined slowly following sound offset. Full horizontal-vertical video image scanning of the entire fiber optic bundle’s face was limited to 18.9 frames/s by the scanning mirror, but isolation and recording of successive individual horizontal scans, done by freezing the vertical scan, yielded 7,550 lines/s, or 132 microseconds for 1 line. Line-scanning revealed that the calcium responses indeed were slow, in the 50-100 ms range. They also were spatially diffuse, suggesting a distributed dendritic origin. [Work supported by JSPS, MEXT Japan, Shandong University, ONR, Capita Foundation.]

Significance of terminal frequency in FM sweeps for bat echolocation

For echolocation of CF-FM bats, the CF component is expected to detect wing-beat of flying insects. However, it also plays an important role to serve as a stable signal carrier from a distant target. Then, once the carrier frequency is removed, echo signal can be easily detected. For this purpose, Doppler-shift compensation and echo amplitude compensation must be conducted to stabilize the signal carrier. What about the FM bats? FM bats also appear to utilize a relatively long pseudo-CF component to detect wing-beats of flying insects. They might also utilize pseudo-CF component for an echo signal carrier. However, Doppler-shift compensation in FM bats has not been reported. In the inferior colliculus, majority of neurons are tuned to the pseudo-CF frequency, 20 kHz for Eptesicus fuscus while 40 kHz for Pipistrellus abramus, which are corresponding to the terminal frequencies of downward FM sweep. Overrepresentation of a particular frequency may enhance frequency discrimination, detection of insect wing-beat. Therefore, we may expect majority of cochlear nerve fibers are also tuned to the pseudo-CF frequency. However, overrepresentation of hair cells for a particular frequency does not appear to be shown. [Research supported by MEXT, Japan and Shandong University, China.]

Distributed acoustic cues for caller identity in macaque vocalization.

Individual primates can be identified by the sound of their voice. Macaques have demonstrated an ability to discern conspecific identity from a harmonically structured ‘coo’ call. Voice recognition presumably requires the integrated perception of multiple acoustic features. However, it is unclear how this is achieved, given considerable variability across utterances. Specifically, the extent to which information about caller identity is distributed across multiple features remains elusive. We examined these issues by recording and analysing a large sample of calls from eight macaques. Single acoustic features, including fundamental frequency, duration and Weiner entropy, were informative but unreliable for the statistical classification of caller identity. A combination of multiple features, however, allowed for highly accurate caller identification. A regularized classifier that learned to identify callers from the modulation power spectrum of calls found that specific regions of spectral–temporal modulation were informative for caller identification. These ranges are related to acoustic features such as the call’s fundamental frequency and FM sweep direction. We further found that the low-frequency spectrotemporal modulation component contained an indexical cue of the caller body size. Thus, cues for caller identity are distributed across identifiable spectrotemporal components corresponding to laryngeal and supralaryngeal components of vocalizations, and the integration of those cues can enable highly reliable caller identification. Our results demonstrate a clear acoustic basis by which individual macaque vocalizations can be recognized.

Strategies for an echolocating FM bat, Pipistrellus abramus, to listen to weak echoes

In Japanese house bat, Pipistrellus abramus, a typical FM-bat, neurophysiological investigation in the inferior colliculus showed that about half of neurons was tuned to the terminal frequency of the downward FM seep or pseudo-CF frequency for searching insects, which was around 40 kHz. Their audiograms determined by the auditory brainstem response (ABR) and the compound action potentials (CAP) of the cochlear nerve also show the lowest threshold or maximum amplitude to be found at around 40 kHz. However, we could not find a sharp notch in their audiogram around 40 kHz, which we have usually found in CF-FM bats at round their reference CF frequency. We examined the peripheral system of Japanese house bat how they extract signals of a flying insect. A particular attention was paid on their terminal frequency of FM sweep or pseudo-CF frequency. [Research supported by MEXT of Japan.]

Active enhancement found in responses of the cochlear nerve to detect weak echoes created by the auditory periphery in Japanese house bat, Pipistrelus abramus

Characteristics of frequency tunings related to echolocation were investigated in an FM bat, Japanese house bat (Pipistrellus abramus). A particular attention was paid on their terminal frequency of FM sweep. When search for preys in the field, they stretch duration of echolocation pulses and reduce FM sweeping range, resulting in pseudo constant frequency pulses. Distribution of best frequency in the neurons in the inferior colliculus indicated that about 50% of neurons appeared to be tuned to the pseudo constant frequency, around 40 kHz. The compound action potentials were recorded from medulla oblongata through a metal telectrode. We hypothesized that the bat has a peripheral system to enhance frequency component of 40 kHz to be detected easier than other frequency components. Active enhancement of 40 kHz frequency component by the outer hair cell and overwhelming number of cochlear nerves in charge of 40 kHz would create low threshold and high resolution sensitivity for frequency range around 40 kHz. ...

Noise induced threshold shifts after noise exposure: Are bats special?

We conducted psychophysical and neurophysiological experiments to test the hypothesis that big brown bats suffer less severe temporary threshold shifts after noise exposure than other small mammals that also hear high frequency sounds. Five big brown bats were trained in psychophysical detection experiments to obtain thresholds to FM sweeps spanning the frequency range of their echolocation calls. Bats were then exposed to 115 dB of broadband noise for one hour, and thresholds re-measured 20 min and 24 hour after exposure. For all bats, threshold elevations at 20 min post-exposure were 3 dB or less, while at 24 hour post-exposure, thresholds were similar to those obtained pre-exposure. Local field potentials were recorded in the cochlear nucleus of anesthetized big brown bats before and after noise exposure. Neural thresholds to FM sweeps and to single tone frequencies were unaffected by noise exposure. These data suggest that big brown bats are an excellent model system to study naturally occurring immunity to noise damage. [Work supported by ONR and the Capita Foundation.]

Characteristics of echolocation system in Japanese house bat, Pipistrellus abramus

Japanese house bats, Pipistrellus abramus, emit harmonically structured downward FM sweeps for echolocation where the fundamental frequency changes from 80 to 40 kHz. Previous studies with an on-board telemetry microphone revealed that they conduct echo-amplitude compensation to stabilize amplitude of returning echoes. When they hunt preys in the field, emitted pulses are prolonged, and the fundamental frequency little change where the terminal fundamental frequency is fixed at about 40 kHz. About 40% of neurons in the inferior colliculus are tuned best to a frequencies range between 35 and 45 kHz, where higher frequency resolution than other frequency ranges is implied and suited for detecting wing beats of insects. However, their audiogram has not yet been known. The present study constructed their audiograms between 4 and 80 kHz by using the auditory brainstem responses evoked by tone pips. Results show that threshold around 40 kHz is lower than other frequencies except for frequency regions around 20 kHz. Findings suggest that Japanese house bats appear to have high sensitivity around 40 kHz, the terminal frequency, and around 20 kHz, corresponding to their communication frequencies. Characteristics of their cochlear microphonics will be discussed. [Work supported by ONR.]

FM-selective Networks in Human Auditory Cortex Revealed Using fMRI and Multivariate Pattern Classification

Frequency modulation (FM) is an acoustic feature of nearly all complex sounds. Directional FM sweeps are especially pervasive in speech, music, animal vocalizations, and other natural sounds. Although the existence of FM-selective cells in the auditory cortex of animals has been documented, evidence in humans remains equivocal. Here we used multivariate pattern analysis to identify cortical selectivity for direction of a multitone FM sweep. This method distinguishes one pattern of neural activity from another within the same ROI, even when overall level of activity is similar, allowing for direct identification of FM-specialized networks. Standard contrast analysis showed that despite robust activity in auditory cortex, no clusters of activity were associated with up versus down sweeps. Multivariate pattern analysis classification, however, identified two brain regions as selective for FM direction, the right primary auditory cortex on the supratemporal plane and the left anterior region of the superior temporal gyrus. These findings are the first to directly demonstrate existence of FM direction selectivity in the human auditory cortex.

Implications of the variety of bat echolocation sounds for understanding biosonar processing

The variety of echolocation sounds used by different species of bats have implications for target ranging. Signals recorded at individual sites reveal species stacked in different frequency bands, perhaps to avoid cross-interference. Search-stage signals include short single-harmonic or multi-harmonic tone-bursts, or very shallow FM bursts. These narrowband sounds have abrupt onsets to evoke phasic on-responses that register echo delay, but with limited acuity. Wider FM sweeps used for searching by other bats evoke on-responses at many more frequencies for better delay acuity. These sound types may signify foraging in the open, within broad spaces bounded relatively remotely by trees or the ground. Intervals between broadcasts are consistent with biosonar operating ranges set by the boundaries of the scene in relation to atmospheric attenuation. Most species make transitions to wider signal bandwidth during interception by increasing FM sweep-width or adding harmonics. Additionally, wideband, multi-harmonic FM sounds are used by species that frequently fly vegetation; they use harmonic processing to suppress surrounding clutter and perceive the path to the front. These observations suggest basic echo-delay processing to determine target range, with increasing bandwidth first to improve delay acuity and then to determine target shape. [Work supported by ONR and NSF.]

High-frequency hearing in seals and sea lions and the implications for detection of ultrasonic coded transmitters

In order to better understand the ability of pinnipeds to detect acoustic signals from ultrasonic coded transmitters (UCTs) commonly used in fisheries research, high-frequency hearing thresholds were obtained from a trained Pacific harbor seal (Phoca vitulina) and a trained California sea lion (Zalophus californianus). Using a 69 kHz, 500 ms, narrow-band FM sweep stimulus, detection thresholds for the harbor seal and the sea lion were determined to be 106 dB and 112 dB re 1 μPa respectively. While the harbor seal threshold falls within the range of existing data, the sea lion threshold is 33 dB lower than expected based on previous reports. This finding indicates that sea lions may be more sensitive to the output of UCTs than previously thought, and allows for the possibility that acoustically tagged fish may be selectively targeted for predation by sea lions as well as seals. These hearing thresholds, combined with ongoing work on the effect of signal duration on high-frequency hearing, will help estimate the ranges at which certain UCTs can be detected by these species. Detection range estimations, in turn, will allow fisheries researchers to better understand how fish survivorship data obtained using UCTs may be skewed by pinniped predation.

Short Cf-Fm and Fm-short CF Calls in the Echolocation Behavior ofPteronotus macleayii(Chiroptera: Mormoopidae)

Echolocation signals were recorded from the Macleay's bat (Pteronotus macleayii) while hunting for insects in the field. Search, approach and terminal phases were identified in the foraging activity of the species. During search phase, P. macleayii emitted calls consisting of a short CF component followed by a downward FM sweep (sCF-FM), typical of the small Pteronotus species. In addition, FM-sCF calls were recorded. In search flight some sequences consisted only of sCF-FM calls while others consisted only of FM-sCF calls. Most sequences, however, combined both call designs. Based on this and previous studies we suggest that sCF-FM and FM-sCF calls will characterize the vocal repertoire of each of the small Pteronotus species. We discuss the relevance of our results for acoustic identification of P. macleayii and the other small Pteronotus in the field.