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P M Narins

Publications and source records attributed to P M Narins.

At least 19 recordsLinked to original sources

Middle ear dynamics in response to seismic stimuli in the Cape golden mole (Chrysochloris asiatica).

The hypertrophied malleus in the middle ear of some golden moles has been assumed to be an adaptation for sensing substrate vibrations by inertial bone conduction, but this has never been conclusively demonstrated. The Cape golden mole (Chrysochloris asiatica) exhibits this anatomical specialization, and the dynamic properties of its middle ear response to vibrations were the subjects of this study. Detailed three-dimensional middle ear anatomy was obtained by x-ray microcomputed tomography (muCT) at a resolution of 12 microm. The ossicular chain exhibits large malleus mass, selective reduction of stiffness and displacement of the center of mass from the suspension points, all favoring low-frequency tuning of the middle ear response. Orientation of the stapes relative to the ossicular chain and the structure of the stapes footplate enable transmission of substrate vibrations arriving from multiple directions to the inner ear. With the long axes of the mallei aligned parallel to the surface, the animal's head was stimulated by a vibration exciter in the vertical and lateral directions over a frequency range from 10 to 600 Hz. The ossicular chain was shown to respond to both vertical and lateral vibrations. Resonant frequencies were found between 71 and 200 Hz and did not differ significantly between the two stimulation directions. Below resonance, the ossicular chain moves in phase with the skull. Near resonance and above, the malleus moves at a significantly larger mean amplitude (5.8+/-2.8 dB) in response to lateral vs vertical stimuli and is 180 degrees out of phase with the skull in both cases. A concise summary of the propagation characteristics of both seismic body (P-waves) and surface (R-waves) is provided. Potential mechanisms by which the animal might exploit the differential response of the ossicular chain to vertical and lateral excitation are discussed in relation to the properties of surface seismic waves.

Animals↗

Ossicular differentiation of airborne and seismic stimuli in the Cape golden mole (Chrysochloris asiatica).

Comparison between the middle ear anatomy of the Cape golden mole (Chrysochloris asiatica), which exhibits a club-shaped malleus head, and the Desert golden mole (Eremitalpa granti), with a ball-shaped malleus head, suggests differences in sensitivity to airborne sound. Scanning laser Doppler vibrometric measurements of the ossicular behavior in response to both vibration and airborne sound were made in C. asiatica. Two distinct vibrational modes were observed. In response to low-frequency vibration (70-200 Hz), the malleus oscillates about the ligament of the short process of the incus, whereas in response to high-frequency airborne sound (1-6 kHz) the ossicular chain rotates about the long axis of malleus. It is proposed that the club-shaped malleus head in C. asiatica constitutes an adaptation towards bimodal hearing-sensitivity to substrate vibrations and airborne sound. Possible functional differences between these two middle ear types are discussed.

Acoustic Stimulation↗

AM representation in green treefrog auditory nerve fibers: neuroethological implications for pattern recognition and sound localization.

In addition to spectral call components, temporal patterns in the advertisement-call envelope of green treefrog males ( Hyla cinerea) provide important cues for female mate choice. Rapid amplitude modulation (AM) with rates of 250-300 Hz is typical for this species' advertisement calls. Here we report data on the encoding of these rapid call modulations by studying the responses of single auditory nerve fibers to two-tone stimuli with envelope periodicities close to those of the natural call. The free-field response properties of 86 nerve fibers were studied from 32 anesthetized males. The accuracy of stimulus envelope coding was quantified using both a Gaussian function fit to the interspike interval histograms derived from the first seven 20-ms stimulus segments, and the vector-strength metric applied to the phase-locked responses. Often, AM encoding in the initial stimulus segment was more faithful than that in its second half. This result may explain why conspecific females prefer calls in which the initial segment is unmasked rather than masked. Both the questions of pattern recognition and localization are discussed, and the data are related to behavioral observations of female choice and localization performance in this species.

Acoustic Stimulation↗

The role of call frequency and the auditory papillae in phonotactic behavior in male Dart-poison frogs Epipedobates femoralis (Dendrobatidae).

Territorial males of the pan-Amazonian Dart-poison frog, Epipedobates femoralis, are known to present stereotypic phonotactic responses to the playback of conspecific and synthetic calls. Fixed site attachment and a long calling period within an environment of little temperature change render this terrestrial and diurnal pan-Amazonian frog a rewarding species for field bioacoustics. In experiments at the field station Aratai, French Guiana, we tested whether the prominent frequency modulation of the advertisement-call notes is critical for eliciting phonotactic responses. Substitution of the natural upward sweep by either a pure tone within the species frequency range or a reverse sweep did not alter the males' phonotactic behavior. Playbacks with artificial advertisement calls embedded in high levels of either low-pass or high-pass masking noise designed to saturate nerve fibers from either the amphibian papilla or basilar papilla showed that male phonotactic behavior in this species is subserved by activation of the basilar papilla of the inner ear.

Acoustic Stimulation↗

Sex differences in the middle ear of the bullfrog (Rana catesbeiana).

Impedance transformation by the middle ear of terrestrial vertebrates is considered to be a function of the ossicular lever apparatus, which increases force and decreases velocity at the stapes footplate relative to the tympanic membrane, and the ratio of tympanic membrane area to stapes footplate area (the area ratio), which increases pressure at the stapes. A recent vibrometric study has found that the velocity ratio between tympanic membrane and stapes footplate is higher in male bullfrogs (Rana catesbeiana) than in females. Although the tympanic membrane area is known to be larger in male bullfrogs, the area ratio has apparently never been compared between the sexes. The hypothesis that a lower area ratio in males helps to compensate for the higher velocity ratio was investigated by comparing tympanic membrane, stapes footplate and operculum areas in frogs of both sexes. Contrary to expectation, the difference in stapes footplate area between males and females is very small, and area ratios are considerably higher in males. Area ratios increase with increasing body size in both sexes. Operculum area does not differ between the sexes. The apparent difference in impedance transformation between male and female frogs might be necessary due to different inner ear impedances, or might reflect serious inadequacies in the conventional models of middle ear function.

Animals↗

Functional consequences of a novel middle ear adaptation in the central African frog Petropedetes parkeri (Ranidae).

During the breeding season, each tympanic membrane of males of the Old World treefrog Petropedetes parkeri is decorated with a single, prominent, fleshy tympanic papilla. The tympanic papilla, located dorsally on the tympanic membrane, is covered by an epidermal surface and is composed of non-ossified, spongiform tissue containing a number of globular, fluid-filled vesicles found at highest density near the papillar tip. These vesicles appear to have exit pores and are probably simple alveolar exocrine glands. Injecting sound into the pressurized vocal cavity of the male and measuring the vibration velocity response of the tympanic membrane revealed that from 0.3 to 2.0 kHz the tympanic papilla velocity amplitude is on average 20 dB lower than that of a point diametrically opposite on the ventral half of the tympanic membrane. The close agreement between the dominant frequency of the call and the frequency of the maximum spectral peak of the Fast Fourier Transform of the impulse response of the eardrum is consistent with the use of the eardrum in this species both as a call receiver and as a call radiator, similar to the function suggested for the eardrum of the male bullfrog Rana catesbeiana. Unexpectedly, surgically removing the tympanic papilla lowered the frequency of the peak vibrational amplitude, testifying to the importance of membrane tension as a dominant factor in the vibratory behavior of the eardrum. During normal positive-pressure breathing, the tympanic papillae move conspicuously, suggesting a possible rôle as a visual signal.

Adaptation, Physiological↗

Mechanics of the inner ear of the bullfrog (Rana catesbeiana): the contact membranes and the periotic canal.

The frog inner ear consists of a complex of fluid-filled membranous sacs and canals containing eight distinct clusters of sensory hair cells. In this study we attempt to delineate the potential pathways for acoustic energy flow toward two of these clusters located within the amphibian papilla and the basilar papilla. Detailed morphological measurements of the periotic canal based on internal casts of the inner ear in the bullfrog (Rana catesbeiana) revealed that it is divided into a wide, tapered section and a narrower section comprised of two branches one short and blind projecting into the endolymphatic space and another longer, terminating in the round window. Additionally, we used laser Doppler velocimetry to record the velocity responses of the contact membranes of the amphibian papilla and basilar papilla. We found that the acoustic energy flow through these two structures is frequency dependent such that the amphibian papilla contact membrane displays a peak velocity amplitude at frequencies less than 500 Hz, whereas the basilar papilla contact membrane velocity response exhibits a maximum above 1,100 Hz. Our data advocate a mechanical substrate underlying the frequency segregation in the auditory nerve fibers innervating the amphibian papilla and the basilar papilla.

Animals↗

A model for energy flow in the inner ear of the bullfrog (Rana catesbeiana).

We present a quantitative mathematical model that represents the main features of the bullfrog inner ear. Calculated responses based on this model predict the observed frequency separation between the amphibian papilla and basilar papilla responses. The origin of this separation can be traced to the effect of the contact membranes on the impedance of the respective paths. Additionally, we calculated the input impedance of the periotic canal and showed that at low frequencies it acts as a bypass for most of the energy entering the ear, shunting it away from the amphibian-basilar papilla complex. As this shunting decreases with increasing frequency, we propose that the periotic canal functions as a protection mechanism to prevent overload of the amphibian papilla and basilar papilla during ventilation and for quasi-static pressure equalization. Our model explains the main features of the empirical data obtained from direct measurement of the amphibian papilla and basilar papilla contact membranes reported in an accompanying paper (this issue).

Animals↗

Hair cells, hearing and hopping: a field guide to hair cell physiology in the frog.

For more than four decades, hearing in frogs has been an important source of information for those interested in auditory neuroscience, neuroethology and the evolution of hearing. Individual features of the frog auditory system can be found represented in one or many of the other vertebrate classes, but collectively the frog inner ear represents a cornucopia of evolutionary experiments in acoustic signal processing. The mechano-sensitive hair cell, as the focal point of transduction, figures critically in the encoding of acoustic information in the afferent auditory nerve. In this review, we provide a short description of how auditory signals are encoded by the specialized anatomy and physiology of the frog inner ear and examine the role of hair cell physiology and its influence on the encoding of sound in the frog auditory nerve. We hope to demonstrate that acoustic signal processing in frogs may offer insights into the evolution and biology of hearing not only in amphibians but also in reptiles, birds and mammals, including man.

Adaptation, Physiological↗

The electrical properties of auditory hair cells in the frog amphibian papilla.

The amphibian papilla (AP) is the principal auditory organ of the frog. Anatomical and neurophysiological evidence suggests that this hearing organ utilizes both mechanical and electrical (hair cell-based) frequency tuning mechanisms, yet relatively little is known about the electrophysiology of AP hair cells. Using the whole-cell patch-clamp technique, we have investigated the electrical properties and ionic currents of isolated hair cells along the rostrocaudal axis of the AP. Electrical resonances were observed in the voltage response of hair cells harvested from the rostral and medial, but not caudal, regions of the AP. Two ionic currents, ICa and IK(Ca), were observed in every hair cell; however, their amplitudes varied substantially along the epithelium. Only rostral hair cells exhibited an inactivating potassium current (IA), whereas an inwardly rectifying potassium current (IK1) was identified only in caudal AP hair cells. Electrically tuned hair cells exhibited resonant frequencies from 50 to 375 Hz, which correlated well with hair cell position and the tonotopic organization of the papilla. Variations in the kinetics of the outward current contribute substantially to the determination of resonant frequency. ICa and IK(Ca) amplitudes increased with resonant frequency, reducing the membrane time constant with increasing resonant frequency. We conclude that a tonotopically organized hair cell substrate exists to support electrical tuning in the rostromedial region of the frog amphibian papilla and that the cellular mechanisms for frequency determination are very similar to those reported for another electrically tuned auditory organ, the turtle basilar papilla.

4-Aminopyridine↗

Potassium currents in auditory hair cells of the frog basilar papilla.

The whole-cell patch-clamp technique was used to identify and characterize ionic currents in isolated hair cells of the leopard frog basilar papilla (BP). This end organ is responsible for encoding the upper limits of a frog's spectral sensitivity (1.25-2.0 kHz in the leopard frog). Isolated BP hair cells are the smallest hair cells in the frog auditory system, with spherical cell bodies typically less than 20 microm in diameter and exhibiting whole-cell capacitances of 4-7 pF. Hair cell zero-current resting potentials (Vz) varied around a mean of -65 mV. All hair cells possessed a non-inactivating, voltage-dependent calcium current (I(Ca)) that activates above a threshold of -55 mV. Similarly all hair cells possessed a rapidly activating, outward, calcium-dependent potassium current (I(K)(Ca)). Most hair cells also possessed a slowly activating, outward, voltage-dependent potassium current (I(K)), which is approximately 80% inactive at the hair cell Vz, and a fast-activating, inward-rectifying potassium current (I(K1)) which actively contributes to setting Vz. In a small subset of cells I(K) was replaced by a fast-inactivating, voltage-dependent potassium current (I(A)), which strongly resembled the A-current observed in hair cells of the frog sacculus and amphibian papilla. Most cells have very similar ionic currents, suggesting that the BP consists largely of one homogeneous population of hair cells. The kinetic properties of the ionic currents present (in particular the very slow I(K)) argue against electrical tuning, a specialized spectral filtering mechanism reported in the hair cells of birds, reptiles, and amphibians, as a contributor to frequency selectivity of this organ. Instead BP hair cells reflect a generalized strategy for the encoding of high-frequency auditory information in a primitive, mechanically tuned, terrestrial vertebrate auditory organ.

Animals↗

Effect of temperature on electrical resonance in leopard frog saccular hair cells.

Leopard frog saccular hair cells exhibit an electrical resonance in response to a depolarizing stimulus that has been proposed to contribute to the tuning properties of the frog sacculus by acting as an electrical band-pass filter. With the whole cell patch-clamp technique, we have investigated the effect of temperature on electrical resonances in isolated saccular hair cells, and we have described the effects of temperature on the currents and channel kinetics underlying electrical resonance. A hair cell's onset resonant frequency in response to a constant depolarizing current pulse increases linearly with temperature at a rate of 11 Hz/1 degrees C, exhibiting a mean Q10 of 1.7 between 15 and 35 degrees C. However, offset resonant frequencies continue to double every 10 degrees C, exhibiting a mean Q10 of 2.1. If steady-state voltage during the stimulus is held constant, all oscillatory frequencies increase with a mean Q10 of 2.1. The average level of steady-state depolarization during a +150-pA depolarizing current pulse decreases with increasing temperature (-6 mV from 15 to 25 degrees C). This temperature-dependent reduction of the steady-state membrane potential causes a shift in the voltage-dependent channel kinetics to slower rates, thus reducing the apparent Q10 for onset resonant frequencies. The peak outward tail current and net steady-state outward current, which is the sum of a voltage-dependent inward calcium current (ICa) and an outward calcium-dependent potassium current (IK(Ca)), increase with temperature, exhibiting a mean Q10 of 1.7 between 15 and 25 degrees C. The activation rate (T1/2) of the outward current exhibits a mean Q10 of 2.3 between 15 and 25 degrees C, while the deactivation rate (taurel) exhibits a mean Q10 of 2.9 over the same temperature range. These results support previous models of the molecular determination of resonant frequency, which have proposed that a combination of IK(Ca) channel kinetics and the overall magnitude of the outward current are primarily responsible for determining the resonant frequency of an isolated hair cell. The robust temperature sensitivity of the hair cell receptor potential contrasts sharply with the temperature-insensitive tuning properties of in vivo saccular nerve fiber recordings. Possible explanations for this discrepancy are discussed.

Animals↗

The use of seismic signals by fossorial southern African mammals: a neuroethological gold mine.

Behavioral adaptations exhibited by two African fossorial mammals for the reception of vibrational signals are discussed. The Namib Desert golden mole (Eremitalpa granti namibensis) is a functionally blind, nocturnal insectivore in the family Chrysochloridae that surface forages nightly in the Namib desert. Both geophone and microphone recordings in the substrate suggest that the golden mole is able to detect termite colonies and other prey items solely using seismic cues. This animal exhibits a hypertrophied malleus, an adaptation favoring detection of low-frequency signals. In a field study of the Cape mole-rat (Georychus capensis), a subterranean rodent in the family Bathyergidae, both seismic and auditory signals were tested for their propagation characteristics. This solitary animal is entirely fossorial and apparently communicates with its conspecifics by drumming its hind legs on the burrow floor. Auditory signals attenuate rapidly in the substrate, whereas vibratory signals generated in one burrow are easily detectable in neighboring burrows. The sensitivity to substrate vibrations in two orders of burrowing mammals suggests that this sense is likely to be widespread within this taxon and may serve as a neuroethological model for understanding the evolution of vibrational communication. Neuroethological implications of these findings are discussed.

Animal Communication↗

Spontaneous otoacoustic emissions in seven frog species.

Spontaneous otoacoustic emissions were screened for in five advanced frog species (Hyla cinerea, n = 10 ears; Hyla chrysoscelis, n = 10; Hyla versicolor, n = 7; Leptodactylus albilabris, n = 2; Rana pipiens pipiens, n = 8), and two primitive frog species (Xenopus laevis, n = 9; Bombina orientalis, n = 12). Emissions were found in 90% of the advanced species' ears, whereas none of the primitive species' ears had emissions. Emission frequencies ranged from 645 Hz to 1680 Hz. The absence of emissions in the primitive species correlates with (1) the absence of a tympanic membrane, and (2) a reduced length of the caudal extension of the amphibian papilla. In eight frogs, the effect of body temperature on emissions was investigated. As a function of temperature, the frequency changed at a rate between 0.009 and 0.091 oct/degree C, and emission levels displayed a complex but consistent behavior. For 9 out of 15 spectral emission peaks encountered during the temperature experiments, the relation between the peak height and peak width was similar to that of an active oscillator.

Acoustic Stimulation↗

Spatial and spectral dependence of the auditory periphery in the northern leopard frog.

We investigated directionalities of eardrum vibration and auditory nerve response in anesthetized northern leopard frogs (Rana pipiens pipiens). Simultaneous measures of eardrum velocities and firing rates from 282 auditory nerve fibers were obtained in response to free-field sounds from eight directions in the horizontal plane. Sound pressure at the external surface of the ipsilateral eardrum was kept constant for each presentation direction (+/- 0.5 dB). Significant effects of sound direction on eardrum velocity were shown in 90% of the cases. Maximum or minimum eardrum velocity was observed more often when sounds were presented from the lateral and posterior fields, or from the anterior and contralateral fields, respectively. Firing rates of 38% of the fibers were significantly affected by sound direction and maximum or minimum firing rate was observed more frequently when sounds were delivered from the lateral fields, or from the anterior and contralateral fields, respectively. Directionality patterns of eardrum velocity and nerve firing also vary with sound frequency. Statistically significant correlation between eardrum velocity and nerve fiber firing rate was demonstrated in only 45% of the fibers, suggesting that sound transmission to the inner ear through extratympanic pathways plays a non-trivial role in the genesis of directionality of auditory nerve responses.

Animals↗

Directional masking of phase locking in the amphibian auditory nerve.

Directional masking in the amphibian auditory periphery was investigated by presenting frogs with a continuous tone from above and a continuous broadband noise from four different horizontal directions. This paradigm mimics the natural situation in which frogs are located in three-dimensional space and interference can and does arise from any direction. Intracellular recordings were made from single auditory-nerve fibers of the anesthetized adult leopard frogs using a dorsal approach. Vector strength (VS) and the mean preferred firing phase (MP) were measured for 94 low-frequency fibers. Thirty-six percent of the fibers demonstrated direction sensitivity of noise masking of VS. Most fibers exhibited a maximum decrease in VS at 90 degrees or 270 degrees noise incident angle and a minimum decrease in VS at 0 degrees or 180 degrees noise incident angle, suggesting higher noise susceptibility to the lateral fields than to the anterior or posterior field. Forty-nine percent of the fibers demonstrated direction sensitivity of noise masking of MP. Maximum shift in MP occurred most often at 90 degrees or 180 degrees noise incident angle, whereas minimum shift in MP occurred most frequently at 0 degrees or 270 degrees noise incident angle, suggesting higher noise susceptibility to the ipsilateral or posterior field than to the contralateral or anterior field. The difference in the directionality patterns of VS and MP suggests different mechanisms underlying noise masking of these two measures of phase locking in the amphibian auditory nerve.

Animals↗

Morphological gradients in sensory hair cells of the amphibian papilla of the frog, Rana pipiens pipiens.

The sensory hair cells of the amphibian papilla (AP) of the northern leopard frog were examined in a light-microscopic analysis. Hair cell length and cross-sectional area were found to vary systematically along the rostro-caudal axis of the endorgan. The AP was readily divided into three morphological regions. Rostrally-located hair cells are tall, cylindrically-shaped cells with large cross-sectional areas and long stereocilia; caudally-located hair cells are short, goblet-shaped cells with small cross-sectional areas and short stereocilia. In the middle region, hair cells exhibit features intermediate to those of hair cells located at the AP extremes. The detailed pattern of changes in hair cell morphology along the endorgan correlates well with its observed tonotopy and may have implications for the intrinsic tuning of the AP.

Animals↗