Short delays and low pulse amplitudes produce widespread activation in the target-distance processing area of auditory cortex of the mustached bat

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)

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Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat

Journal of Neurophysiology ◽

10.1152/jn.1985.53.4.1109 ◽

1985 ◽

Vol 53 (4) ◽

pp. 1109-1145 ◽

Cited By ~ 70

Author(s):

N. Suga ◽

K. Tsuzuki

Keyword(s):

Auditory Cortex ◽

Frequency Analysis ◽

Frequency Tuning ◽

Neural Basis ◽

Single Tone ◽

Tuning Curves ◽

Mustached Bat ◽

Essential Components ◽

High Stimulus ◽

Pulse Echo

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)

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Representation of Biosonar Information in the Auditory Cortex of the Mustached Bat, with Emphasis on Representation of Target Velocity Information

Advances in Vertebrate Neuroethology ◽

10.1007/978-1-4684-4412-4_40 ◽

1983 ◽

pp. 829-867 ◽

Cited By ~ 17

Author(s):

Nobuo Suga ◽

Hideto Niwa ◽

Ikuo Taniguchi

Keyword(s):

Auditory Cortex ◽

Target Velocity ◽

Mustached Bat ◽

Velocity Information

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Erratum: Modulation of cochlear hair cells by the auditory cortex in the mustached bat

Nature Neuroscience ◽

10.1038/nn0202-182b ◽

2002 ◽

Vol 5 (2) ◽

pp. 182-182

Keyword(s):

Auditory Cortex ◽

Hair Cells ◽

Cochlear Hair Cells ◽

Mustached Bat

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Cell Types in the Mustached Bat Auditory Cortex

Brain Behavior and Evolution ◽

10.1159/000113626 ◽

1994 ◽

Vol 43 (2) ◽

pp. 79-91 ◽

Cited By ~ 20

Author(s):

Douglas C. Fitzpatrick ◽

O.W. Henson, Jr.

Keyword(s):

Auditory Cortex ◽

Cell Types ◽

Mustached Bat

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Postnatal Maturation of Primary Auditory Cortex in the Mustached Bat, Pteronotus parnellii

Journal of Neurophysiology ◽

10.1152/jn.00517.2009 ◽

2010 ◽

Vol 103 (5) ◽

pp. 2339-2354 ◽

Cited By ~ 8

Author(s):

M. Vater ◽

E. Foeller ◽

E. C. Mora ◽

F. Coro ◽

I. J. Russell ◽

...

Keyword(s):

Auditory Cortex ◽

Cortical Neurons ◽

Second Harmonic ◽

Tuning Curve ◽

Primary Auditory Cortex ◽

Constant Frequency ◽

Low Frequencies ◽

Postnatal Maturation ◽

Mustached Bat ◽

Pteronotus Parnellii

The primary auditory cortex (AI) of adult Pteronotus parnellii features a foveal representation of the second harmonic constant frequency (CF2) echolocation call component. In the corresponding Doppler-shifted constant frequency (DSCF) area, the 61 kHz range is over-represented for extraction of frequency-shift information in CF2 echoes. To assess to which degree AI postnatal maturation depends on active echolocation or/and reflects ongoing cochlear maturation, cortical neurons were recorded in juveniles up to postnatal day P29, before the bats are capable of active foraging. At P1-2, neurons in posterior AI are tuned sensitively to low frequencies (22–45 dB SPL, 28–35 kHz). Within the prospective DSCF area, neurons had insensitive responses (>60 dB SPL) to frequencies <40 kHz and lacked sensitive tuning curve tips. Up to P10, when bats do not yet actively echolocate, tonotopy is further developed and DSCF neurons respond to frequencies of 51–57 kHz with maximum tuning sharpness ( Q10dB) of 57. Between P11 and 20, the frequency representation in AI includes higher frequencies anterior and dorsal to the DSCF area. More multipeaked neurons (33%) are found than at older age. In the oldest group, DSCF neurons are tuned to frequencies close to 61 kHz with Q10dB values ≤212, and threshold sensitivity, tuning sharpness and cortical latencies are adult-like. The data show that basic aspects of cortical tonotopy are established before the bats actively echolocate. Maturation of tonotopy, increase of tuning sharpness, and upward shift in the characteristic frequency of DSCF neurons appear to strongly reflect cochlear maturation.

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Delay-tuned combination-sensitive neurons in the auditory cortex of the vocalizing mustached bat

Journal of Neurophysiology ◽

10.1152/jn.1988.59.2.623 ◽

1988 ◽

Vol 59 (2) ◽

pp. 623-635 ◽

Cited By ~ 36

Author(s):

M. Kawasaki ◽

D. Margoliash ◽

N. Suga

Keyword(s):

Auditory Cortex ◽

Sound Pressure ◽

Pressure Level ◽

Target Range ◽

Mustached Bat ◽

Equivalent Effect ◽

Loud Speaker ◽

Cochlear Microphonic Potentials ◽

Self Stimulation ◽

Delay Tuning

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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