Postnatal Development of Cochlear Function in the Mustached Bat, Pteronotus parnellii

2003 ◽  
Vol 90 (4) ◽  
pp. 2261-2273 ◽  
Author(s):  
M. Kössl ◽  
E. Foeller ◽  
M. Drexl ◽  
M. Vater ◽  
E. Mora ◽  
...  

Postnatal development of the mustached bat's cochlea was studied by measuring cochlear microphonic and compound action potentials. In adults, a cochlear resonance is involved in enhanced tuning to the second harmonic constant frequency component (CF2) of their echolocation calls at ∼61 kHz This resonance is present immediately after birth in bats that do not yet echolocate. Its frequency is lower (46 kHz) and the corresponding threshold minimum of cochlear microphonic potentials is broader than in adults. Long-lasting ringing of the cochlear microphonic potential after tone stimulus offset that characterizes the adult auditory response close to CF2 is absent in newborns. In the course of the first 5 postnatal weeks, there is a concomitant upward shift of CF2 and the frequency of cochlear threshold minima. Up to the end of the third postnatal week, sensitivity of auditory threshold minima and the Q value of the cochlear resonance increase at a fast rate. Between 2 and 4 wk of age, two cochlear microphonic threshold minima are found consistently in the CF2 range that differ in their level-dependent dynamic growth behavior and are 1.5–5.7 kHz apart from each other. In older animals, there is a single minimum that approaches adult tuning in its sharpness. The data provide evidence to show that during maturation of the cochlea, the frequency and the sensitivity of the threshold minimum associated with CF2 increases and that these increases are associated with the fusion of two resonances that are partly dissociated in developing animals.

1983 ◽  
Vol 50 (5) ◽  
pp. 1182-1196 ◽  
Author(s):  
A. Asanuma ◽  
D. Wong ◽  
N. Suga

The orientation sound emitted by the Panamanian mustached bat, Pteronotus parnellii rubiginosus, consists of four harmonics. The third harmonic is 6-12 dB weaker than the predominant second harmonic and consists of a long constant-frequency component (CF3) at about 92 kHz and a short frequency-modulated component (FM3) sweeping from about 92 to 74 kHz. Our primary aim is to examine how CF3 and FM3 are represented in a region of the primary auditory cortex anterior to the Doppler-shifted constant-frequency (DSCF) area. Extracellular recordings of neuronal responses from the unanesthetized animal were obtained during free-field stimulation of the ears with pure tones. FM sounds, and signals simulating their orientation sounds and echoes. Response properties of neurons and tonotopic and amplitopic representations were examined in the primary and the anteroventral nonprimary auditory cortex. In the anterior primary auditory cortex, neurons responded strongly to single pure tones but showed no facilitative responses to paired stimuli. Neurons with best frequencies from 110 to 90 kHz were tonotopically organized rostrocaudally, with higher frequencies located more rostrally. Neurons tuned to 92-94 kHz were overpresented, whereas neurons tuned to sound between 64 and 91 kHz were rarely found. Consequently a striking discontinuity in frequency representation from 91 to 64 kHz was found across the anterior DSCF border. Most neurons exhibited monotonic impulse-count functions and responded maximally to sound pressure level (SPL). There were also neurons that responded best to weak sounds but unlike the DSCF area, amplitopic representation was not found. Thus, the DSCF area is quite unique not only in its extensive representation of frequencies in the second harmonic CF component but also in its amplitopic representation. The anteroventral nonprimary auditory cortex consisted of neurons broadly tuned to pure tones between 88 and 99 kHz. Neither tonotopic nor amplitopic representation was observed. Caudal to this area and near the anteroventral border of the DSCF area, a small cluster of FM-FM neurons sensitive to particular echo delays was identified. The responses of these neurons fluctuated significantly during repetitive stimulation.


1994 ◽  
Vol 188 (1) ◽  
pp. 115-129 ◽  
Author(s):  
A W Keating ◽  
O W Henson ◽  
M M Henson ◽  
W C Lancaster ◽  
D H Xie

Quantitative data for Doppler-shift compensation by Pteronotus parnellii parnellii were obtained with a device which propelled the bats at constant velocities over a distance of 12 m. The bats compensated for Doppler shifts at all velocities tested (0.1-5.0 ms-1). The main findings were (1) that compensation was usually accomplished by a progressive lowering of the approximately 61 kHz second harmonic constant-frequency component of emitted sounds in small frequency steps (93 +/- 72 Hz); (2) that the time needed to reach a steady compensation level averaged 514 +/- 230 ms and the number of pulses required to reach full compensation averaged 10.78 +/- 5.16; (3) that the animals compensated to hold the echo (reference) frequency at a value that was slightly higher than the resting frequency and slightly lower than the cochlear resonance frequency; (4) that reference frequency varied as a function of velocity, the higher the velocity of the animal, the higher was the reference frequency (slope 55 Hz m-1s-2); and (5) that the mean reference frequency was always an undercompensation. The average amount of undercompensation was 15.8%. There was a significant difference (P < or = 0.005) in Doppler-shift compensation data collected at velocities that differed by 0.1 ms-1. A velocity difference of 0.1 ms-1 corresponds to a Doppler-shift difference of about 35 Hz in the approximately 61 kHz signals reaching the ear.


1987 ◽  
Vol 58 (4) ◽  
pp. 643-654 ◽  
Author(s):  
N. Suga ◽  
H. Niwa ◽  
I. Taniguchi ◽  
D. Margoliash

1. In the mustached bat, Pteronotus parnellii, the "resting" frequency of the constant-frequency component of the second harmonic (CF2) of the orientation sound (biosonar signal) is different among individuals within a range from 59.69 to 63.33 kHz. The standard deviation of CF2 resting frequency is 0.091 kHz on the average for individual bats. The male's CF2 resting frequency (61.250 +/- 0.534 kHz, n = 58) is 1.040 kHz lower than the female's (62.290 +/- 0.539 kHz, n = 58) on the average. Females' resting frequencies measured in December are not different from those measured in April when almost all of them are pregnant. Therefore, the orientation sound is sexually dimorphic. 2. In the DSCF (Doppler-shifted CF processing) area of the auditory cortex, tonotopic representation differs among individual bats. The higher the CF2 resting frequency of the bat's own sound, the higher the frequencies represented in the DSCF area of that bat. There is a unique match between the tonotopic representation and the CF2 resting frequency. This match indicates that the auditory cortex is "personalized" for echolocation and that the CF2 resting frequency is like a signature of the orientation sound. 3. If a bat's resting frequency is normalized to 61.00 kHz, the DSCF area overrepresents 60.6-62.3 kHz. The central region of this overrepresented band is 61.1-61.2 kHz. This focal band matches the "reference" frequency to which the CF2 frequency of a Doppler-shifted echo is stabilized by Doppler-shift compensation. 4. Since DSCF neurons are extraordinarily sharply tuned in frequency, the personalization of the auditory cortex or system is not only suited for the detection of wing beats of insects, but also for the reduction of the masking effect on echolocation of consepecific's biosonar signals. 5. Because the orientation sound is sexually dimorphic and the auditory cortex is personalized, the tonotopic representation of the auditory cortex is also sexually dimorphic.


1991 ◽  
Vol 66 (6) ◽  
pp. 1951-1964 ◽  
Author(s):  
D. C. Fitzpatrick ◽  
N. Suga ◽  
H. Misawa

1. FM-FM neurons in the auditory cortex of the mustached bat, Pteronotus parnellii, are specialized to process target range. They respond when the terminal frequency-modulated component (TFM) of a biosonar pulse is paired with the TFM of the echo at a particular echo delay. Recently, it has been suggested that the initial FM components (IFMs) of biosonar signals may also be important for target ranging. To examine the possible role of IFMs in target ranging, we characterized the properties of IFMs and TFMs in biosonar pulses emitted by bats swung on a pendulum. We then studied responses of FM-FM neurons to synthesized biosonar signals containing IFMs and TFMs. 2. The mustached bat's biosonar signal consists of four harmonics, of which the second (H2) is the most intense. Each harmonic has an IFM in addition to a constant-frequency component (CF) and a TFM. Therefore each pulse potentially consists of 12 components, IFM1-4, CF1-4, and TFM1-4. The IFM sweeps up while the TFM sweeps down. 3. The IFM2 and TFM2 depths (i.e., bandwidths) were measured in 217 pulses from four animals. The mean IFM2 depth was much smaller than the mean TFM2 depth, 2.87 +/- 1.52 (SD) kHz compared with 16.27 +/- 1.08 kHz, respectively. The amplitude of the IFM2 continuously increased throughout its duration and was always less than the CF2 amplitude, whereas the TFM2 was relatively constant in amplitude over approximately three-quarters of its duration and was often the most intense part of the pulse. The maximum amplitude of the IFM2 was, on average, 11 dB smaller than that of the TFM2. Because range resolution increases with depth and the maximum detectable range increases with signal amplitude, the IFMs are poorly suited for ranging compared with the TFMs. 4. FM-FM neurons (n = 77) did not respond or responded very poorly to IFMs with depths and intensities similar to those emitted on the pendulum. The mean IFM2 depth at which a just-noticeable response appeared was 4.48 +/- 1.98 kHz. Only 14% of the pulses emitted on the pendulum had IFM2 depths that exceeded the mean IFM2 depth threshold of FM-FM neurons. 5. Most FM-FM neurons responded to IFMs that had depths comparable with those of TFMs. However, when all parameters were adjusted to optimize the response to TFMs and then readjusted to maximize the response to IFMs, 52% of 27 neurons tested responded significantly better to the optimal TFMs than to the optimal IFMs (P less than 0.05, t test).(ABSTRACT TRUNCATED AT 400 WORDS)


2010 ◽  
Vol 103 (5) ◽  
pp. 2339-2354 ◽  
Author(s):  
M. Vater ◽  
E. Foeller ◽  
E. C. Mora ◽  
F. Coro ◽  
I. J. Russell ◽  
...  

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.


2008 ◽  
Vol 100 (6) ◽  
pp. 3285-3304 ◽  
Author(s):  
Stuart D. Washington ◽  
Jagmeet S. Kanwal

Neurons in the Doppler-shifted constant frequency processing (DSCF) area in the primary auditory cortex of mustached bats, Pteronotus parnellii, are multifunctional, responding both to echolocation and communication sounds. Simultaneous presentation of a DSCF neuron's best low and high frequencies (BFlow and BFhigh, respectively) facilitates its response. BFlow corresponds to a frequency in the frequency-modulated (FM) component of the first harmonic in the echolocation pulse, and BFhigh corresponds to the constant frequency (CF) component in the second harmonic of the echo. We systematically varied the slopes, bandwidths, and central frequencies of FMs traversing the BFhigh region to arrive at the “best FM” for single DSCF neurons. We report that nearly half (46%) of DSCF neurons preferred linear FMs to CFs and average response magnitude to FMs was not significantly less ( P = 0.08) than that to CFs at BFhigh when each test stimulus was paired with a CF at BFlow. For linear FMs ranging in slope from 0.04 to 4.0 kHz/ms and in bandwidth from 0.44 to 7.88 kHz, the majority of DSCF neurons preferred upward (55%) to downward (21%) FMs. Central frequencies of the best FMs were typically close to but did not always match a neuron's BFhigh. Neurons exhibited combination-sensitivity to “call fragments” (calls that were band-pass filtered in the BFhigh region) paired with their BFlow. Our data show a close match between the modulation direction of a neuron's best FM and that of its preferred call fragment. These response properties show that DSCF neurons extract multiple parameters of FMs and are specialized for processing both FMs for communication and CFs for echolocation.


2011 ◽  
Vol 106 (6) ◽  
pp. 3119-3128 ◽  
Author(s):  
Silvio Macías ◽  
Emanuel C. Mora ◽  
Julio C. Hechavarría ◽  
Manfred Kössl

We studied duration tuning in neurons of the inferior colliculus (IC) of the mustached bat. Duration-tuned neurons in the IC of the mustached bat fall into three main types: short (16 of 136), band (34 of 136), and long (29 of 136) pass. The remaining 51 neurons showed no selectivity for the duration of sounds. The distribution of best durations was double peaked with maxima around 3 and 17 ms, which correlate with the duration of the short frequency-modulated (FM) and the long constant-frequency (CF) signals emitted by Pteronotus parnellii. Since there are no individual neurons with a double-peaked duration response profile, both types of temporal processing seem to be well segregated in the IC. Most short- and band-pass units with best frequency in the CF2 range responded to best durations > 9 ms (66%, 18 of 27 units). However, there is no evidence for a bias toward longer durations as there is for neurons tuned to the frequency range of the FM component of the third harmonic, where 83% (10 of 12 neurons) showed best durations longer than 9 ms. In most duration-tuned neurons, response areas as a function of stimulus duration and intensity showed either V or U shape, with duration tuning retained across the range of sound levels tested. Duration tuning was affected by changes in sound pressure level in only six neurons. In all duration-tuned neurons, latencies measured at the best duration were longer than best durations, suggesting that behavioral decisions based on analysis of the duration of the pulses would not be expected to be complete until well after the stimulus has occurred.


1993 ◽  
Vol 69 (5) ◽  
pp. 1713-1724 ◽  
Author(s):  
N. Kuwabara ◽  
N. Suga

1. The biosonar pulse of the mustached bat, Pteronotus parnellii parnellii, consists of four harmonics of a constant-frequency component (CF1-4) followed by a frequency-modulated component (FM1-4). FM-FM combination-sensitive neurons in the auditory cortex and the medical geniculate body (MGB) show facilitative responses to certain combinations of FM components in a pulse-echo pair. They are tuned to particular delays of echo FMn (EFMn) (n = 2, 3, or 4) from pulse FM1 (PFM1). The neural mechanisms for creating their response properties involve delay lines, coincidence detection, and multiplication. Coincidence detection and multiplication take place in the MGB. It is not yet known where and how delay lines are created. The first aim of the present studies is to examine whether delay lines are created by subthalamic nuclei. FM-FM neurons are tuned to not only echo delays but also echo amplitudes. Therefore, the second aim of the present studies is to examine the extent to which amplitude selectivity is created by subthalamic nuclei. Responses of single nerve fibers to acoustic stimuli were recorded from the brachium of the inferior colliculus (BIC) using tungsten wire microelectrodes, and their response latencies and best amplitudes were measured. 2. All BIC fibers responded strongly to single tone bursts. No FM-FM combination-sensitive neurons were found in the BIC. The best frequencies of BIC fibers were predominantly within the frequency ranges of four harmonics of the species-specific biosonar pulse. 3. The response latencies of BIC fibers tuned to FM1 were more diverse (3.5-15.0 ms) than those of BIC fibers tuned to FMn (3.8-6.5 ms). This difference in latency distribution was independent of stimulus amplitude. These data are consistent with the theory that delay lines utilized by FM-FM neurons are created by neurons tuned to the "FM1 frequency," and indicate that the delay lines are mostly, if not all, created in a subthalamic nucleus or nuclei. 4. The best amplitudes of BIC fibers tuned to FM1 or CF1 were 63.2 +/- 4.5 (SE) dB SPL, and those of BIC fibers tuned to FMn or CFn were 48.2 +/- 10.7 dB SPL. The distribution of the best amplitudes of BIC fibers were very similar to those of FM-FM and CF/CF neurons in the MGB. These data indicate that the amplitude selectivity of thalamic FM-FM and CF/CF neurons is mainly a product of a subthalamic nucleus or nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)


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