Differences in response properties of neurons between two delay-tuned areas in the auditory cortex of the mustached bat

1993 ◽  
Vol 69 (5) ◽  
pp. 1700-1712 ◽  
Author(s):  
H. Edamatsu ◽  
N. Suga
Keyword(s):  
Auditory Cortex ◽  
Poor Response ◽  
Target Range ◽  
Terminal Phase ◽  
Sound Pulse ◽  
Response Properties ◽  
Tuning Curves ◽  
Mustached Bat ◽  
Echo Delay ◽  
Delay Tuning

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)

Distribution of combination-sensitive neurons in the ventral fringe area of the auditory cortex of the mustached bat

1989 ◽  
Vol 61 (1) ◽  
pp. 202-207 ◽  
Author(s):  
H. Edamatsu ◽  
M. Kawasaki ◽  
N. Suga
Keyword(s):  
Auditory Cortex ◽  
Functional Organization ◽  
Target Range ◽  
Sound Pulse ◽  
Constant Frequency ◽  
Mustached Bat ◽  
Essential Components ◽  
Tritiated Amino Acids ◽  
Pulse Echo ◽  
Echo Delay

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)

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

1988 ◽  
Vol 59 (2) ◽  
pp. 623-635 ◽  
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.

Combination-sensitive neurons in the ventroanterior area of the auditory cortex of the mustached bat

1988 ◽  
Vol 60 (6) ◽  
pp. 1908-1923 ◽  
Author(s):  
K. Tsuzuki ◽  
N. Suga
Keyword(s):  
Auditory Cortex ◽  
Functional Organization ◽  
Primary Auditory Cortex ◽  
Great Majority ◽  
Signal Pulse ◽  
Constant Frequency ◽  
Response Properties ◽  
Tuning Curves ◽  
Mustached Bat ◽  
Anterior Division

1. Because the ventroanterior (VA) area is one of the target areas of the FM-FM area in the auditory cortex of the mustached bat, Pteronotus parnellii parnellii, response properties of combination-sensitive neurons in this area were studied with constant-frequency (CF) tones, frequency-modulated (FM) sounds, and sounds similar to the bat's biosonar signal (pulse), which consisted of long CF components (CF1-4) and short FM components (FM1-4). CF1-4 and FM1-4 are the components in the four harmonics (H1-4) of the pulse. 2. Combination-sensitive neurons are clustered in a small area immediately anteroventral to the Doppler-shifted CF processing (DSCF) area and posteroventral to the anterior division of the primary auditory cortex. Because this cluster in the VA area is small, it was difficult to record a sufficient number of combination-sensitive neurons to explore the functional organization of the cluster, but it was found that the response properties of these VA neurons were unique. 3. Combination-sensitive neurons in the VA area are tuned to particular combinations of signal elements similar to the first and second harmonics of the pulse and/or echo. Unlike neurons in the FM-FM, dorsal fringe (DF), and CF/CF areas, no neurons in the VA area are tuned to the signal elements in the first and third or fourth harmonics. 4. The great majority of combination-sensitive neurons in the VA area can not be easily classified into either FM-FM or CF/CF neurons, because they show facilitative responses to combinations of CF1/CF2, FM1-FM2, and FM1-CF2. Therefore, they are called H1-H2 neurons. In the FM-FM and CF/CF areas, all the neurons could be easily classified as FM-FM or CF/CF. This uniqueness of H1-H2 neurons is related to the fact that their best frequencies for facilitation are predominantly between 61.0 and 62.0 kHz, i.e., within the frequency range of stabilized Doppler-shifted echo CF2. 5. In addition to 27 H1-H2 neurons, 7 FM1-FM2 neurons were also recorded in the VA area. The best delays of these H1-H2 and FM1-FM2 neurons measured with FM1-FM2 pairs are between 1 and 10 ms. Unlike neurons in the FM-FM and DF areas, their delay-tuning curves are very broad, even if their best delays are short, and extend beyond zero delay to several millisecond "negative" delays of the FM2 from the FM1, i.e., several millisecond delays of the FM1 from the FM2.(ABSTRACT TRUNCATED AT 400 WORDS)

Comparison of properties of cortical echo delay-tuning in the short-tailed fruit bat and the mustached bat

2010 ◽  
Vol 197 (5) ◽  
pp. 605-613 ◽  
Author(s):  
Cornelia Hagemann ◽  
Marianne Vater ◽  
Manfred Kössl
Keyword(s):  
Fruit Bat ◽  
Mustached Bat ◽  
Echo Delay ◽  
Delay Tuning

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

1985 ◽  
Vol 53 (4) ◽  
pp. 1109-1145 ◽  
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)

NMDA-mediated facilitation in the echo-delay tuned areas of the auditory cortex of the mustached bat

1997 ◽  
Vol 110 (1-2) ◽  
pp. 219-228 ◽  
Author(s):  
Atsushi Tanahashi ◽  
Junsei Horikawa ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Mustached Bat ◽  
Echo Delay

Multiple time axes for representation of echo delays in the auditory cortex of the mustached bat

1986 ◽  
Vol 55 (4) ◽  
pp. 776-805 ◽  
Author(s):  
N. Suga ◽  
J. Horikawa
Keyword(s):  
Auditory Cortex ◽  
Tuning Curve ◽  
Electrophysiological Study ◽  
Great Majority ◽  
Major Axis ◽  
Essential Elements ◽  
Multiple Time ◽  
Sound Pulse ◽  
Constant Frequency ◽  
Mustached Bat

The properties of the orientation sound (pulse) of the Jamaican mustached bat, Pteronotus parnellii parnellii is the same as the Panamanian mustached bat, P.p. rubiginosus. It consists of four harmonics, each containing a long constant-frequency (CF) component followed by a short frequency-modulated (FM) component. Thus, there are eight components in total: CF1-4 and FM1-4. The combination-sensitive area of the auditory cortex in P.p. parnellii consists of two major divisions (FM-FM and CF/CF areas) as in P.p. rubiginosus. The FM-FM area projects to the dorsal fringe (DF) and other areas. Response latencies of neurons in the DF area are longer than those in the FM-FM area. The distribution of latencies is unimodal for the FM-FM area, but bimodal for the DF area. In this electrophysiological study of the response properties of neurons in the DF and FM-FM areas, our aim was to find out how signal processing might be different between the two areas. Both the FM-FM and DF areas consist of three types of FM-FM combination-sensitive neurons: FM1-FM2, FM1-FM3, and FM1-FM4. They do not respond or respond poorly to pulse alone, echo alone, single CF tones or single FM sounds. But they show strong facilitation of response to the echo when it is delivered with particular delays from the pulse. The essential elements in the pulse-echo pair for facilitation are the FM1 of the pulse and FM2 or FM3 or FM4 of the echo. In both the FM-FM and DF areas, the great majority of neurons show short-lasting facilitation, and other neurons show long-lasting facilitation. FM-FM neurons are tuned to particular echo delays, i.e., target ranges. In both the FM-FM and DF areas, the width of a delay-tuning curve is linearly related to the value of a best delay. There is no sign that processing of range information is more specialized in the DF area than the FM-FM area. In both the FM-FM and DF areas, three types of FM-FM neurons form independent clusters. Along the major axis of each cluster, best delays for facilitative responses of neurons systematically change according to the loci of the neurons. The more posterior the location, the longer the best delay is. Therefore, there are six time (i.e., range) axes in total. The time axis in the DF area is shorter than that in the FM-FM area.(ABSTRACT TRUNCATED AT 400 WORDS)

Delay-Tuned Neurons in the Inferior Colliculus of the Mustached Bat: Implications for Analyses of Target Distance

1999 ◽  
Vol 82 (3) ◽  
pp. 1326-1338 ◽  
Author(s):  
Christine V. Portfors ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Tuning Curve ◽  
Central Nucleus ◽  
Harmonic Frequency ◽  
High Frequency Signal ◽  
Response Properties ◽  
Mustached Bat ◽  
Medial Geniculate ◽  
Higher Harmonic ◽  
Delay Tuning

We examined response properties of delay-tuned neurons in the central nucleus of the inferior colliculus (ICC) of the mustached bat. In the mustached bat, delay-tuned neurons respond best to the combination of the first-harmonic, frequency-modulated (FM1) sweep in the emitted pulse and a higher harmonic frequency-modulated (FM2, FM3 or FM4) component in returning echoes and are referred to as FM-FM neurons. We also examined H1-CF2 neurons. H1-CF2 neurons responded to simultaneous presentation of the first harmonic (H1) in the emitted pulse and the second constant frequency (CF2) component in returning echoes. These neurons served as a comparison as they are thought to encode different features of sonar targets than FM-FM neurons. Only 7% of our neurons (14/198) displayed a single excitatory tuning curve. The rest of the neurons (184) displayed complex responses to sounds in two separate frequency bands. The majority (51%, 101) of neurons were facilitated by the combination of specific components in the mustached bat’s vocalizations. Twenty-five percent showed purely inhibitory interactions. The remaining neurons responded to two separate frequencies, without any facilitation or inhibition. FM-FM neurons (69) were facilitated by the FM1 component in the simulated pulse and a higher harmonic FM component in simulated echoes, provided the high-frequency signal was delayed the appropriate amount. The delay producing maximal facilitation (“best delay”) among FM-FM neurons ranged between 0 and 20 ms, corresponding to target distances ≤3.4 m. Sharpness of delay tuning varied among FM-FM neurons with 50% delay widths between 2 and 13 ms. On average, the facilitated responses of FM-FM neurons were 104% greater than the sum of the responses to the two signals alone. In comparing response properties of delay-tuned, FM-FM neurons in the ICC with those in the medial geniculate body (MGB) from other studies, we find that the range of best delays, sharpness of delay tuning and strength of facilitation are similar in the ICC and MGB. This suggests that by the level of the IC, the basic response properties of FM-FM neurons are established, and they do not undergo extensive transformations with ascending auditory processing.

scholarly journals Natural echolocation sequences evoke echo-delay selectivity in the auditory midbrain of the FM bat, Eptesicus fuscus

2018 ◽  
Vol 120 (3) ◽  
pp. 1323-1339 ◽  
Author(s):  
Silvio Macías ◽  
Jinhong Luo ◽  
Cynthia F. Moss
Keyword(s):  
Inferior Colliculus ◽  
Sweep Rate ◽  
Eptesicus Fuscus ◽  
Target Range ◽  
Temporal Patterning ◽  
Stimulus Context ◽  
Constant Frequency ◽  
New Findings ◽  
Echo Delay ◽  
Delay Tuning

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.

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