scholarly journals Echo-acoustic flow shapes object representation in spatially complex acoustic scenes

2017 ◽  
Vol 117 (6) ◽  
pp. 2113-2124 ◽  
Author(s):  
Wolfgang Greiter ◽  
Uwe Firzlaff

Echolocating bats use echoes of their sonar emissions to determine the position and distance of objects or prey. Target distance is represented as a map of echo delay in the auditory cortex (AC) of bats. During a bat’s flight through a natural complex environment, echo streams are reflected from multiple objects along its flight path. Separating such complex streams of echoes or other sounds is a challenge for the auditory system of bats as well as other animals. We investigated the representation of multiple echo streams in the AC of anesthetized bats ( Phyllostomus discolor) and tested the hypothesis that neurons can lock on echoes from specific objects in a complex echo-acoustic pattern while the representation of surrounding objects is suppressed. We combined naturalistic pulse/echo sequences simulating a bat’s flight through a virtual acoustic space with extracellular recordings. Neurons could selectively lock on echoes from one object in complex echo streams originating from two different objects along a virtual flight path. The objects were processed sequentially in the order in which they were approached. Object selection depended on sequential changes of echo delay and amplitude, but not on absolute values. Furthermore, the detailed representation of the object echo delays in the cortical target range map was not fixed but could be dynamically adapted depending on the temporal pattern of sonar emission during target approach within a simulated flight sequence. NEW & NOTEWORTHY Complex signal analysis is a challenging task in sensory processing for all animals, particularly for bats because they use echolocation for navigation in darkness. Recent studies proposed that the bat’s perceptional system might organize complex echo-acoustic information into auditory streams, allowing it to track specific auditory objects during flight. We show that in the auditory cortex of bats, neurons can selectively respond to echo streams from specific objects.

1989 ◽  
Vol 61 (1) ◽  
pp. 202-207 ◽  
Author(s):  
H. Edamatsu ◽  
M. Kawasaki ◽  
N. Suga

1. The orientation sound (pulse) of the mustached bat, Pteronotus parnellii parnellii, consists of long constant-frequency components (CF1-4) and short frequency-modulated components (FM1-4). The auditory cortex of this bat contains several combination-sensitive areas: FM-FM, DF, VA, VF, and CF/CF. The FM-FM area consists of neurons tuned to a combination of the pulse FM1 and the echo FMn (n = 2, 3, or 4) and has an echo-delay (target-range) axis. Our preliminary anatomical studies with tritiated amino acids suggest that the FM-FM area projects to the dorsal fringe (DF) area, which in turn projects to the ventral fringe (VF) area. The aim of our study was to characterize the response properties of VF neurons and to explore the functional organization of the VF area. Acoustic stimuli delivered to the bats were CF tones, FM sounds, and their combinations mimicking the pulse emitted by the mustached bat and the echo. 2. Like the FM-FM and DF areas, the VF area is composed of three types of FM-FM combination-sensitive neurons: FM1-FM2, FM1-FM3, and FM1-FM4. These neurons show little or no response to a pulse alone, echo alone, single CF tone or single FM sound. They do, however, show a strong facilitative response to a pulse-echo pair with a particular echo delay. The essential components in the pulse-echo pair for facilitation are the FM1 of the pulse and the FMn of the echo.(ABSTRACT TRUNCATED AT 250 WORDS)


2010 ◽  
Vol 103 (1) ◽  
pp. 322-333 ◽  
Author(s):  
Cornelia Hagemann ◽  
Karl-Heinz Esser ◽  
Manfred Kössl

Topographic cortical representation of echo delay, the cue for target range, is an organizational feature implemented in the auditory cortices of certain bats dedicated to catch flying insects. Such cortical echo-delay maps provide a calibrated neural representation of object spatial distance. To assess general requirements for echo-delay computations, cortical delay sensitivity was examined in the short-tailed fruit bat Carollia perspicillata that uses frequency-modulated (FM) echolocation signals. Delay-tuned neurons with temporal specificity comparable to those of insectivorous bats are located within the high-frequency (HF) field of the auditory cortex. All recorded neurons in the HF field respond well to single pure-tone and FM-FM stimulus pairs. The neurons respond to identical FM harmonic components in echolocation pulse and delayed echo (e.g., FM2-FM2). Their characteristic delays (CDs) for low echo amplitudes range between 1 and 24 ms, which is comparable to other bat species. Maps of the topography of FM-FM neurons show that they are distributed across the entire HF area and organized along a rostrocaudal echo-delay axis representing object distance. Rostrally located neurons tuned to delays of 2–8 ms are overrepresented (66% of CDs). Neurons with longer delays (≥10 ms) are located throughout the caudal half of the HF field. The delay-sensitive chronotopic area covers ∼3.3 mm in rostrocaudal and ∼3.7 mm in dorsoventral direction, which is comparable or slightly larger than the size of cortical delay-tuned areas in insectivorous constant frequency bats, the only other bat species for which cortical chronotopy has been demonstrated. This indicates that chronotopic cortical organization is not only used exclusively for precise insect localization in constant frequency bats but could also be of advantage for general orientation tasks.


1993 ◽  
Vol 69 (5) ◽  
pp. 1700-1712 ◽  
Author(s):  
H. Edamatsu ◽  
N. Suga

1. The orientation sound (pulse) of the mustached bat, Pteronotus parnellii parnellii, consists of four harmonics (H1-4), each containing a long constant-frequency component (CF1-4) followed by a short frequency-modulated component (FM1-4). The auditory cortex of this species contains several "combination-sensitive" areas: FM-FM, dorsal fringe (DF), ventral fringe (VF), CF/CF, and H1-H2. The FM-FM, DF, and VF areas each consist of neurons tuned to particular delays of echo FMn (n = 2, 3, or 4) from pulse FM1, and have an echo-delay (target-range) axis. This delay axis is from 0.4 to approximately 18 ms in the FM-FM area, to approximately 9 ms in the DF area, and to approximately 5 ms in the VF area. Therefore we hypothesized that the VF area was more specialized for the processing of range information in the terminal phase of echolocation than was the FM-FM area. The aim of our present studies was to find differences in response properties between neurons with best delays shorter than 6 ms in the VF and FM-FM areas and thus to test our hypothesis. 2. In the terminal phase of target-directed flight, the rate of pulse emission becomes higher, pulse duration (in particular, CF duration) becomes shorter, echo delay becomes shorter, and echoes (both the CF and FM components) are less Doppler shifted. Therefore, a "temporal-pattern-simulating (TPS)" stimulus was designed to mimic the train of pulse-echo pairs that would be heard by the bat during the terminal phase, and responses of single neurons to the TPS stimulus and other types of stimuli were recorded from the VF and FM-FM areas of the auditory cortex of unanesthetized bats with a tungsten-wire microelectrode. 3. Best delays of the neurons studied range between 0.9 and 5.5 ms (2.64 +/- 0.72 ms, N = 181) for the VF area, and between 0.6 and 6.0 ms (3.64 +/- 1.14, N = 144) for the FM-FM area. More neurons in the VF area than those in the FM-FM area showed no response or a poor response to the TPS stimulus. Therefore VF neurons are less suited than neurons in the FM-FM area for processing target ranges in the terminal phase of target-directed flight. Facilitative delay-tuning curves were commonly sandwiched between inhibitory delay-tuning curves. The lack of response or poor response to the TPS stimulus can be explained by this inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (3) ◽  
pp. 1084-1100 ◽  
Author(s):  
S. P. Dear ◽  
N. Suga

1. The auditory midbrain in Eptesicus contains delay-tuned neurons that encode target range. Most delay-tuned neurons respond poorly to tones or individual frequency-modulated (FM) sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned. The index of facilitation (IF), a coefficient measuring combination sensitivity for individual delay-tuned neurons, ranged from 0.14 to 1.0, with an average of 0.64 +/- 0.24 (mean +/- SD). Of the 33 facilitated responses from 29 neurons, 23 (70%) exhibited IFs > 0.5, which corresponds to a facilitated response 3 times greater than the sum of the responses to individual pulse and echoes. Thus the responses of midbrain delay-tuned neurons are highly combination sensitive. 2. The response of midbrain delay-tuned neurons is phasic, with an average of 0.7 +/- 0.4 action potentials elicited per optimal pulse-echo pair. Thus midbrain delay-tuned neurons in Eptesicus act as probability encoders. 3. The distribution of best echo delays (BDs) of midbrain delay-tuned neurons ranged from 8 to 30 ms. As an ensemble, midbrain delay-tuned neurons encode target ranges of 138-516 cm. There is a basic correspondence between the physiologically determined span of midbrain BDs between 8 and 30 ms and the behaviorally determined borders of the approach (8- to 17-ms echo delay) and search stages (17- to 30-ms echo delay) of the insect pursuit sequence. Midbrain delay-tuned neurons can be separated into two subpopulations on the basis of the difference in distributions of the echo best amplitude (EBA) tuning at BD. The BDs of one subpopulation correspond to the span of search stage echo delays, and the BDs of the other subpopulation correspond to the span of approach stage echo delays. 4. EBAs of neurons in each subpopulation are tailored to the specific perceptual requirements of the corresponding behavioral stage. EBAs of midbrain neurons tuned to echo delays between 17 and 30 ms (N = 12) correspond to the search stage and are suited to the requirements of target detection. EBAs of midbrain neurons tuned to echo delays between 17 and 30 ms (N = 21) correspond to the approach stage and are suited to the requirements of target size discrimination. 5. The best FM sweeps for the pulse (PFM) and echo (EFM) were determined for each midbrain neuron. PFMs appear to cluster at frequencies corresponding to the three harmonic peaks in the emitted pulse power spectra.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 72 (1) ◽  
pp. 366-379 ◽  
Author(s):  
W. G. Paschal ◽  
D. Wong

1. The little brown bat, Myotis lucifugus, employs biosonar pulses containing broadband frequency -modulated (FM) sounds of only one harmonic during the initial phases of echolocation. Neurons throughout the auditory cortex exhibit delay-dependent facilitation to artificial pulses and echoes at particular echo delays. Extracellular unit recordings of these delay-sensitive neurons determined the essential frequency components in the sound pair and their relative timing for evoking maximum facilitation. 2. The entire 60-kHz sweep of both the simulated pulse and echo were divided into four equal spectral quarters (Ist, IInd, IIIrd, and IVth), each linearly sweeping 15 kHz downward in 1 ms, to determine the spectral parts essential for maximal facilitation. Maximal facilitation was evoked equally by pulse-echo pairs in which the sound components consisted of either the entire 60-kHz FM sweeps or only the essential quarters. Most neurons required the IVth quarter of the pulse and the echo for delay sensitivity. This is consistent with the hypothesis that the essential quarters swept excitatory frequencies just above inhibitory frequencies. 3. The spectral and temporal contributions to delay sensitivity were examined independently. The spectral content for each spectral quarter of echo was varied in echo delay, and the sound-pair responses were compared. Maximal facilitation in individual delay-sensitive neurons required both a specific part of the echo spectrum and a specific echo delay. 4. The FM sweeps of the essential pulse and echo quarters were further narrowed to their minimum bandwidth, and the essential pulse frequencies (EPFs) and essential echo frequencies (EEFs) were determined. Both the EPFs and EEFs averaged approximately 8 kHz in FM bandwidth and represented different spectral parts of the echolocation pulse emitted by this FM bat. All neurons showed delay sensitivity to search stimuli in which pulse-echo stimuli consisted of 15-kHz FM pairs. 5. Delay sensitivity in virtually all neurons required pulse and echo components whose essential frequencies differed. However, some spectral overlap was found between the pulse and echo in 39% of these neurons. The majority of neurons (81%) required a pulse and echo in which their mean frequencies differed by>or = 16 kHz. This includes neurons with pulse and echo overlapping spectrally and those with sound components showing no overlap but separated by a relatively small frequency range. 6. The facilitative frequency-tuning curves of individual neurons were measured with their essential pulse and echo frequencies.(ABSTRACT TRUNCATED AT 400 WORDS)


1985 ◽  
Vol 53 (4) ◽  
pp. 1109-1145 ◽  
Author(s):  
N. Suga ◽  
K. Tsuzuki

For echolocation the mustached bat, Pteronotus parnellii, emits complex orientation sounds (pulses), each consisting of four harmonics with long constant-frequency components (CF1-4) followed by short frequency-modulated components (FM1-4). The CF signals are best suited for target detection and measurement of target velocity. The CF/CF area of the auditory cortex of this species contains neurons sensitive to pulse-echo pairs. These CF/CF combination-sensitive neurons extract velocity information from Doppler-shifted echoes. In this study we electrophysiologically investigated the frequency tuning of CF/CF neurons for excitation, facilitation, and inhibition. CF1/CF2 and CF1/CF3 combination-sensitive neurons responded poorly to individual signal elements in pulse-echo pairs but showed strong facilitation of responses to pulse-echo pairs. The essential components in the pairs were CF1 of the pulse and CF2 or CF3 of the echo. In 68% of CF/CF neurons, the frequency-tuning curves for facilitation were extremely sharp for CF2 or CF3 and were "level-tolerant" so that the bandwidths of the tuning curves were less than 5.0% of best frequencies even at high stimulus levels. Facilitative tuning curves for CF1 were level tolerant only in 6% of the neurons studied. CF/CF neurons were specialized for fine analysis of the frequency relationship between two CF sounds regardless of sound pressure levels. Some CF/CF neurons responded to single-tone stimuli. Frequency-tuning curves for excitation (responses to single-tone stimuli) were extremely sharp and level tolerant for CF2 or CF3 in 59% of CF1/CF2 neurons and 70% of CF1/CF3 neurons. Tuning to CF1 was level tolerant in only 9% of these neurons. Sharp level-tolerant tuning may be the neural basis for small difference limens in frequency at high stimulus levels. Sharp level-tolerant tuning curves were sandwiched between broad inhibitory areas. Best frequencies for inhibition were slightly higher or lower than the best frequencies for facilitation and excitation. We thus conclude that sharp level-tolerant tuning curves are produced by inhibition. The extent to which neural sharpening occurred differed among groups of neurons tuned to different frequencies. The more important the frequency analysis of a particular component in biosonar signals, the more pronounced the neural sharpening. This was in addition to the peripheral specialization for fine frequency analysis of that component. The difference in bandwidth or quality factor between the excitatory tuning curves of peripheral neurons and the facilitative and excitatory tuning curves of CF/CF neurons was larger at higher stimulus levels.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (5) ◽  
pp. 1988-2009 ◽  
Author(s):  
S. P. Dear ◽  
J. Fritz ◽  
T. Haresign ◽  
M. Ferragamo ◽  
J. A. Simmons

1. In Eptesicus the auditory cortex, as defined by electrical activity recorded from microelectrodes in response to tone bursts, FM sweeps, and combinations of FM sweeps, encompasses an average cortical surface area of 5.7 mm2. This area is large with respect to the total cortical surface area and reflects the importance of auditory processing to this species of bat. 2. The predominant pattern of organization in response to tone bursts observed in each cortex is tonotopic, with three discernible divisions revealed by our data. However, although cortical best-frequency (BF) maps from most of the individual bats are similar, no two maps are identical. The largest division contains an average of 84% of the auditory cortical surface area, with BF tonotopically mapped from high to low along the anteroposterior axis and is part of the primary auditory cortex. The medium division encompasses an average of 13% of the auditory cortical surface area, with highly variable BF organization across bats. The third region is the smallest, with an average of only 3% of auditory cortical surface area and is located at the anterolateral edge of the cortex. This region is marked by a reversal of the tonotopic axis and a restriction in the range of BFs as compared with the larger, tonotopically organized division. 3. A population of cortical neurons was found (n = 39) in which each neuron exhibited two BF threshold minima (BF1 and BF2) in response to tone bursts. These neurons thus have multipeaked frequency threshold tuning curves. In Eptesicus the majority of multipeaked frequency-tuned neurons (n = 27) have threshold minima at frequencies that correspond to a harmonic ratio of three-to-one. In contrast, the majority of multipeaked neurons in cats have threshold minima at frequencies in a ratio of three-to-two. A three-to-one harmonic ratio corresponds to the "spectral notches" produced by interference between overlapping echoes from multiple reflective surfaces in complex sonar targets. Behavioral experiments have demonstrated the ability of Eptesicus to use spectral interference notches for perceiving target shape, and this subpopulation of multipeaked frequency-tuned neurons may be involved in coding of spectral notches. 4. The auditory cortex contains delay-tuned neurons that encode target range (n = 99). Most delay-tuned neurons respond poorly to tones or individual FM sweeps and require combinations of FM sweeps. They are combination sensitive and delay tuned.(ABSTRACT TRUNCATED AT 400 WORDS)


2019 ◽  
Vol 121 (4) ◽  
pp. 1501-1512 ◽  
Author(s):  
Stephen Gareth Hörpel ◽  
Uwe Firzlaff

Bats use a large repertoire of calls for social communication. In the bat Phyllostomus discolor, social communication calls are often characterized by sinusoidal amplitude and frequency modulations with modulation frequencies in the range of 100–130 Hz. However, peaks in mammalian auditory cortical modulation transfer functions are typically limited to modulation frequencies below 100 Hz. We investigated the coding of sinusoidally amplitude modulated sounds in auditory cortical neurons in P. discolor by constructing rate and temporal modulation transfer functions. Neuronal responses to playbacks of various communication calls were additionally recorded and compared with the neurons’ responses to sinusoidally amplitude-modulated sounds. Cortical neurons in the posterior dorsal field of the auditory cortex were tuned to unusually high modulation frequencies: rate modulation transfer functions often peaked around 130 Hz (median: 87 Hz), and the median of the highest modulation frequency that evoked significant phase-locking was also 130 Hz. Both values are much higher than reported from the auditory cortex of other mammals, with more than 51% of the units preferring modulation frequencies exceeding 100 Hz. Conspicuously, the fast modulations preferred by the neurons match the fast amplitude and frequency modulations of prosocial, and mostly of aggressive, communication calls in P. discolor. We suggest that the preference for fast amplitude modulations in the P. discolor dorsal auditory cortex serves to reliably encode the fast modulations seen in their communication calls. NEW & NOTEWORTHY Neural processing of temporal sound features is crucial for the analysis of communication calls. In bats, these calls are often characterized by fast temporal envelope modulations. Because auditory cortex neurons typically encode only low modulation frequencies, it is unclear how species-specific vocalizations are cortically processed. We show that auditory cortex neurons in the bat Phyllostomus discolor encode fast temporal envelope modulations. This property improves response specificity to communication calls and thus might support species-specific communication.


2000 ◽  
Vol 83 (5) ◽  
pp. 2723-2739 ◽  
Author(s):  
Gregg H. Recanzone ◽  
Darren C. Guard ◽  
Mimi L. Phan ◽  
Tien-I K. Su

Lesion studies have indicated that the auditory cortex is crucial for the perception of acoustic space, yet it remains unclear how these neurons participate in this perception. To investigate this, we studied the responses of single neurons in the primary auditory cortex (AI) and the caudomedial field (CM) of two monkeys while they performed a sound-localization task. Regression analysis indicated that the responses of ∼80% of neurons in both cortical areas were significantly correlated with the azimuth or elevation of the stimulus, or both, which we term “spatially sensitive.” The proportion of spatially sensitive neurons was greater for stimulus azimuth compared with stimulus elevation, and elevation sensitivity was primarily restricted to neurons that were tested using stimuli that the monkeys also could localize in elevation. Most neurons responded best to contralateral speaker locations, but we also encountered neurons that responded best to ipsilateral locations and neurons that had their greatest responses restricted to a circumscribed region within the central 60° of frontal space. Comparing the spatially sensitive neurons with those that were not spatially sensitive indicated that these two populations could not be distinguished based on either the firing rate, the rate/level functions, or on their topographic location within AI. Direct comparisons between the responses of individual neurons and the behaviorally measured sound-localization ability indicated that proportionally more neurons in CM had spatial sensitivity that was consistent with the behavioral performance compared with AI neurons. Pooling the responses across neurons strengthened the relationship between the neuronal and psychophysical data and indicated that the responses pooled across relatively few CM neurons contain enough information to account for sound-localization ability. These data support the hypothesis that auditory space is processed in a serial manner from AI to CM in the primate cerebral cortex.


1988 ◽  
Vol 59 (2) ◽  
pp. 623-635 ◽  
Author(s):  
M. Kawasaki ◽  
D. Margoliash ◽  
N. Suga

1. FM-FM neurons in the auditory cortex of the mustached bat are sensitive to a pair of frequency-modulated (FM) sounds that simulates an FM component of the orientation sound and an FM component of the echo. These neurons are tuned to particular delays between the two FM components, suggesting an encoding of target range information. The response properties of these FM-FM neurons, however, have previously been studied only with synthesized orientation sounds and echoes delivered from a loud-speaker as substitutes for the bat's own orientation sounds and corresponding echoes. In this study, the combination sensitivity and delay tuning of FM-FM neurons were examined while the bat was actively vocalizing. 2. When the bat produced orientation sounds in an anechoic environment, or synthesized single FM echoes were delivered to a silent bat, the FM-FM neurons showed weak or no response. In contrast, when synthesized FM echoes were delivered with a particular delay from the FM component of the vocalized orientation sounds, the FM-FM neurons exhibited strong facilitative responses. 3. In both the vocalizing bats and the silent bats with substituted synthesized orientation sounds, all FM-FM neurons tested responded preferentially to the same echo harmonic (FM2, FM3, or FM4). 4. In vocalizing bats, FM-FM neurons showed maximum response to an echo FM component delivered with a particular delay (best delay) from an FM component in the orientation sound. Best delays measured with vocalized orientation sounds were nearly the same as those measured with synthesized orientation sounds. 5. The equivalent effect of a vocalized orientation sound and a synthesized FM1 component on the activity of FM-FM neurons indicates that, during echolocation, the FM1 component in the vocalized orientation sound stimulates the auditory system and conditions the FM-FM neurons to be sensitive to echoes with particular delays from the vocalized orientation sounds. 6. The amount of vocal self-stimulation to the inner ear by the bat's own vocalized sounds was measured by recording cochlear microphonic potentials (CMs). Spectral analysis of CM indicated that the amount of vocal self-stimulation by each harmonic of an orientation sound was equivalent to a sound of 70 dB sound pressure level (SPL) for the first harmonic (H1), 91 dB SPL for H2, 83 dB SPL for H3, and 70 dB SPL for H4, when the amplitude of the vocalized sound was 117 dB SPL at 5 cm in front of the bat's mouth.


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