Chronotopically Organized Target-Distance Map in the Auditory Cortex of the Short-Tailed Fruit Bat

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.

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)


2018 ◽  
Vol 120 (3) ◽  
pp. 1323-1339 ◽  
Author(s):  
Silvio Macías ◽  
Jinhong Luo ◽  
Cynthia F. Moss

Echolocating bats must process temporal streams of sonar sounds to represent objects along the range axis. Neuronal echo-delay tuning, the putative mechanism of sonar ranging, has been characterized in the inferior colliculus (IC) of the mustached bat, an insectivorous species that produces echolocation calls consisting of constant frequency and frequency modulated (FM) components, but not in species that use FM signals alone. This raises questions about the mechanisms that give rise to echo-delay tuning in insectivorous bats that use different signal designs. To investigate whether stimulus context may account for species differences in echo-delay selectivity, we characterized single-unit responses in the IC of awake passively listening FM bats, Eptesicus fuscus, to broadcasts of natural sonar call-echo sequences, which contained dynamic changes in signal duration, interval, spectrotemporal structure, and echo-delay. In E. fuscus, neural selectivity to call-echo delay emerges in a population of IC neurons when stimulated with call-echo pairs presented at intervals mimicking those in a natural sonar sequence. To determine whether echo-delay selectivity also depends on the spectrotemporal features of individual sounds within natural sonar sequences, we studied responses to computer-generated echolocation signals that controlled for call interval, duration, bandwidth, sweep rate, and echo-delay. A subpopulation of IC neurons responded selectively to the combination of the spectrotemporal structure of natural call-echo pairs and their temporal patterning within a dynamic sonar sequence. These new findings suggest that the FM bat’s fine control over biosonar signal parameters may modulate IC neuronal selectivity to the dimension of echo-delay. NEW & NOTEWORTHY Echolocating bats perform precise auditory temporal computations to estimate their distance to objects. Here, we report that response selectivity of neurons in the inferior colliculus of a frequency modulated bat to call-echo delay, or target range tuning, depends on the temporal patterning and spectrotemporal features of sound elements in a natural echolocation sequence. We suggest that echo responses to objects at different distances are gated by the bat’s active control over the spectrotemporal patterning of its sonar emissions.


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.


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)


1992 ◽  
Vol 68 (5) ◽  
pp. 1613-1623 ◽  
Author(s):  
H. Riquimaroux ◽  
S. J. Gaioni ◽  
N. Suga

1. The Jamaican mustached bat uses a biosonar signal (pulse) with eight major components: four harmonics each consisting of a long constant frequency (CF1-4) component followed by a short frequency-modulated (FM1-4) component. While flying, the bat adjusts the frequency of its pulse so as to maintain the CF2 of the Doppler-shifted echo at a frequency to which its cochlea is very sharply tuned. This Doppler shift (DS) compensation likely is mediated or influenced by the Doppler-shifted CF (DSCF) processing area of the primary auditory cortex, which only represents frequencies in the range of echo CF2s (60.6 to 62.3 kHz when the "resting" frequency of the CF2 is 61.0 kHz). 2. We trained four bats to discriminate between different trains of paired tone bursts that mimicked a bat's pulse CF2 and the accompanying echo CF2. The frequency of these CF2s ranged between 61.0 and 64.0 kHz. A discriminated shock avoidance procedure response was employed using a leg flexion. For one stimulus, the S+, the pulse and echo CF2s were the same frequency (delta f = 0, i.e., no Doppler shift). A leg flexion during the S+ turned off both the S+ and the scheduled shock. For a second stimulus, the S-, the echo CF2 was 0.05, 0.1, 0.3, 0.5, or 2.0 kHz higher than the pulse CF2. A delta f of 0.05 kHz was a frequency difference of 0.08%. No shock followed the S-, and leg flexions had no consequences. Correct responses consisted of a leg flexion during the S+ and no flexion during the S-; these responses were added together to compute the percentage of correct responses. When a bat correctly responded at better than 75% for all the delta f s, muscimol, a potent agonist of gamma-aminobutyric acid, was bilaterally applied to inactivate the DSCF area. Performance on each delta f discrimination was then measured. 3. Initial attempts to condition the bats to flex their legs to the CF tones mimicking part of the natural pulses and echoes failed. When broad-band noise bursts were substituted, however, the conditioned response was rapidly established. The noise band-width was gradually reduced and then replaced with the CF tones. Discrimination training with the tone burst trains then commenced. Throughout this procedure, the bats maintained their responding to the stimuli. The bats typically required approximately 20-30 sessions to perform consistently (> or = 75% correct responses) a discrimination involving a 2 kHz delta f.(ABSTRACT TRUNCATED AT 400 WORDS)


2002 ◽  
Vol 88 (1) ◽  
pp. 540-543 ◽  
Author(s):  
John J. Foxe ◽  
Glenn R. Wylie ◽  
Antigona Martinez ◽  
Charles E. Schroeder ◽  
Daniel C. Javitt ◽  
...  

Using high-field (3 Tesla) functional magnetic resonance imaging (fMRI), we demonstrate that auditory and somatosensory inputs converge in a subregion of human auditory cortex along the superior temporal gyrus. Further, simultaneous stimulation in both sensory modalities resulted in activity exceeding that predicted by summing the responses to the unisensory inputs, thereby showing multisensory integration in this convergence region. Recently, intracranial recordings in macaque monkeys have shown similar auditory-somatosensory convergence in a subregion of auditory cortex directly caudomedial to primary auditory cortex (area CM). The multisensory region identified in the present investigation may be the human homologue of CM. Our finding of auditory-somatosensory convergence in early auditory cortices contributes to mounting evidence for multisensory integration early in the cortical processing hierarchy, in brain regions that were previously assumed to be unisensory.


2020 ◽  
Vol 123 (2) ◽  
pp. 695-706
Author(s):  
Lu Luo ◽  
Na Xu ◽  
Qian Wang ◽  
Liang Li

The central mechanisms underlying binaural unmasking for spectrally overlapping concurrent sounds, which are unresolved in the peripheral auditory system, remain largely unknown. In this study, frequency-following responses (FFRs) to two binaurally presented independent narrowband noises (NBNs) with overlapping spectra were recorded simultaneously in the inferior colliculus (IC) and auditory cortex (AC) in anesthetized rats. The results showed that for both IC FFRs and AC FFRs, introducing an interaural time difference (ITD) disparity between the two concurrent NBNs enhanced the representation fidelity, reflected by the increased coherence between the responses evoked by double-NBN stimulation and the responses evoked by single NBNs. The ITD disparity effect varied across frequency bands, being more marked for higher frequency bands in the IC and lower frequency bands in the AC. Moreover, the coherence between IC responses and AC responses was also enhanced by the ITD disparity, and the enhancement was most prominent for low-frequency bands and the IC and the AC on the same side. These results suggest a critical role of the ITD cue in the neural segregation of spectrotemporally overlapping sounds. NEW & NOTEWORTHY When two spectrally overlapped narrowband noises are presented at the same time with the same sound-pressure level, they mask each other. Introducing a disparity in interaural time difference between these two narrowband noises improves the accuracy of the neural representation of individual sounds in both the inferior colliculus and the auditory cortex. The lower frequency signal transformation from the inferior colliculus to the auditory cortex on the same side is also enhanced, showing the effect of binaural unmasking.


2010 ◽  
Vol 197 (5) ◽  
pp. 605-613 ◽  
Author(s):  
Cornelia Hagemann ◽  
Marianne Vater ◽  
Manfred Kössl

2017 ◽  
Author(s):  
Krishna C. Puvvada ◽  
Jonathan Z. Simon

AbstractThe ability to parse a complex auditory scene into perceptual objects is facilitated by a hierarchical auditory system. Successive stages in the hierarchy transform an auditory scene of multiple overlapping sources, from peripheral tonotopically-based representations in the auditory nerve, into perceptually distinct auditory-objects based representation in auditory cortex. Here, using magnetoencephalography (MEG) recordings from human subjects, both men and women, we investigate how a complex acoustic scene consisting of multiple speech sources is represented in distinct hierarchical stages of auditory cortex. Using systems-theoretic methods of stimulus reconstruction, we show that the primary-like areas in auditory cortex contain dominantly spectro-temporal based representations of the entire auditory scene. Here, both attended and ignored speech streams are represented with almost equal fidelity, and a global representation of the full auditory scene with all its streams is a better candidate neural representation than that of individual streams being represented separately. In contrast, we also show that higher order auditory cortical areas represent the attended stream separately, and with significantly higher fidelity, than unattended streams. Furthermore, the unattended background streams are more faithfully represented as a single unsegregated background object rather than as separated objects. Taken together, these findings demonstrate the progression of the representations and processing of a complex acoustic scene up through the hierarchy of human auditory cortex.Significance StatementUsing magnetoencephalography (MEG) recordings from human listeners in a simulated cocktail party environment, we investigate how a complex acoustic scene consisting of multiple speech sources is represented in separate hierarchical stages of auditory cortex. We show that the primary-like areas in auditory cortex use a dominantly spectro-temporal based representation of the entire auditory scene, with both attended and ignored speech streams represented with almost equal fidelity. In contrast, we show that higher order auditory cortical areas represent an attended speech stream separately from, and with significantly higher fidelity than, unattended speech streams. Furthermore, the unattended background streams are represented as a single undivided background object rather than as distinct background objects.


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