Peter Martin Narins - US grants

The overall goal of the proposed research is to understand how the vertebrate auditory system encodes time-varying biologically significant information in the presence of natural and artificially produced background noise. This will be accomplished by examining the temporal resolving ability of single auditory fibers and single cells in the central auditory system of anurans (frogs and toads) in the presence of narrowband, broadband, and natural background noise of various levels. Specifically, we shall address the following questions: (1) What are the absolute limits of phase-locking of single auditory neurons to sinusoidal stimuli and to what extent does phase-locking deteriorate in the presence of masking noise? (2) How is temporal coding affected by previous exposure to high-level noise (such as occurs in the animals' habitat)? (3) What are the temporal integration characteristics of the peripheral auditory system of anurans, are they affected by the level and character of the background noise, and do they reflect the characteristics of the animal's vocalizations? and finally, (4) How does the relative spatial orientation between signal and masker affect the temporal resolving ability of single cells? We believe these studies will provide much needed insight into the neural substrate underlying species-specific communication in adverse (noisy) environments, and that this work will serve as a model for the understanding fundamental problems of human speech perception in the presence of noise.

The overall goal of the proposed research is to understand how the vertebrate auditory system encodes time-varying biologically significant information in the presence of natural and artificially produced background noise. This will be accomplished by examining the temporal resolving ability of single auditory fibers and single cells in the central auditory system of anurans (frogs and toads) in the presence of narrowband, broadband, and natural background noise of various levels. Specifically, we shall address the following questions: (1) What are the absolute limits of phase-locking of single auditory neurons to sinusoidal stimuli and to what extent does phase-locking deteriorate in the presence of masking noise? (2) How is temporal coding affected by previous exposure to high-level noise (such as occurs in the animals' habitat)? (3) What are the temporal integration characteristics of the peripheral auditory system of anurans, are they affected by the level and character of the background noise, and do they reflect the characteristics of the animal's vocalizations? and finally, (4) How does the relative spatial orientation between signal and masker affect the temporal resolving ability of single cells? We believe these studies will provide much needed insight into the neural substrate underlying species-specific communication in adverse (noisy) environments, and that this work will serve as a model for the understanding fundamental problems of human speech perception in the presence of noise.

The overall goal of the proposed research is a richer understanding of the structural and physiological bases of frequency selectivity in the vertebrate auditory system. In particular, the primary objectives of the proposed research are to gain an understanding and appreciation of the mechanical and electrical factors underlying frequency resolution in the vertebrate auditory system, and to provide further insights into the mechanisms underlying stimulus interactions which affect tuning in the vertebrate inner ear. To accomplish the first objective, we intend to perform a series of three detailed investigations in order to (a) directly measure the motion of the tectorial membrane partition in response to sound and thus more precisely define the role of this structure in frequency analysis, (b) characterize in situ the temperature dependence of the tectorial membrane partition in its response to pure tones, and (c) systematically study the membrane properties of anatomically-defined hair cells from the amphibian papilla, and to relate these properties to the known tonotopic organization of the organ. To accomplish the second objective, we shall (d) extend our investigation of the interactions between acoustic and seismic stimuli on the recently characterized bimodal fibers in the eighth nerve, and (e) quantify the extent to which the extratympanic pathways to the inner ear play a role in sculpting the tuned responses of the peripheral auditory system. We believe that the data that result from this combined structure-function and neurethological approach will be rich in implications regarding the anatomical and neural substrate underlying the processing of complex sounds, and that this work will serve as a model for understanding fundamental problems of human speech perception in noisy environments.

The overall goal of the proposed research is a quantitative description of the structural and physiological constraints on low-frequency selectivity in the vertebrate auditory system. In particular, the primary objectives of the proposed research are to gain an understanding and appreciation of the mechanical and electrical factors underlying airborne, substrate-borne and combination (bimodal) stimulus reception, and to provide further insight into the mechanisms underlying stimulus interactions which affect tuning in the vertebrate inner ear. To accomplish these objectives, a series of five detailed investigations will be performed in order to a (a) directly measure the motion of the middle ear ossicles in amphibians in response to airborne sound, substrate-borne vibration and bimodal stimulation, and thus more precisely define the role of these structures in low-frequency reception, (b) characterize the airborne and seismic response properties of the middle ear ossicles of two other "low- frequency" animals- the common and golden mole- and thus extend our observations to fossorial mammals, (c) quantify the extent to which the tectorial membrane responds to low-frequency sound and vibration in order to elucidate the role of this structure in bimodal processing, (d) systematically compare synaptic release in low-frequency (bimodal) and high-frequency (unimodal) hair cells from the amphibian papilla by tracking correlated capacitance changes in response to depolarization, and (e) extend our investigation of the nonlinear interactions between acoustic and seismic stimuli to the bimodal fibers in the eighth nerve. The data that result from this integrative structure-functional and neuroethological approach will be rich in implications regarding the anatomical and neural substrates underlying the processing of sound-vibration complexes; thus this work is expected to provide a framework for understanding the relationship between air-conducted and bone-conducted sound transmission in animals, including humans.

[unreadable] DESCRIPTION (provided by applicant): The overall goal of our laboratory is a richer understanding of the structural and physiological bases of the frequency selectivity or tuning in the vertebrate auditory system. Driven by a knowledge of the animal's acoustic behavior in its natural habitat, our primary objectives for the proposed research are threefold: (1) to apply modern techniques to provide new insights into the physiological and biophysical mechanisms underlying the localization of airborne sound and substrate-borne vibration in the vertebrate ear, (2) to gain an understanding and appreciation of the mechanisms underlying the electrical and mechanical cellular processes that modulate and sculpt low-frequency selectivity in the auditory periphery, and (3) to explore the physiological bases underlying the newly-discovered remarkable ultrasonic sensitivity in the amphibian ear. To accomplish these objectives, a series of four detailed investigations will be performed in order to (a) directly measure the motion of the middle ear ossicles in a "low-frequency" animal, the golden mole, in order to characterize the directional responses of the middle ear ossicles to airborne and seismic stimuli- and thus extend our observations to a subterranean seismic specialist, (b) systematically compare both receptor pharmacology and ionic current kinetics in the same hair cell preparation to directly test the effects of exogenous agents on tuning properties of low-frequency hair cells, (c) examine the calcium-calmodulin- dependent contractile mechanism mediating slow motility in response to extracellular stimuli in vertebrate hair cells, and (d) characterize the tuning of the peripheral auditory system of a high-frequency specialist and to determine the mechanisms subserving this tuning. The data that result will be rich in implications regarding the processing of airborne sound and substrate vibration as well as the role of efferent-mediated feedback in frequency tuning. Thus, this work is expected to provide a framework for understanding both airborne and bone-conducted sound transmission and tuning in animals, including humans. Of major current interest is the putative role of the efferent system in the genesis of frequency selectivity and protection against noise overstimulation. Ultimately, our research may lead to new therapeutic approaches to treatment of hyperacusis and noise-induced tinnitus, two known syndromes in which efferent system malfunction has been implicated. [unreadable] [unreadable] [unreadable]

Victoria Arch
Proposal # IOS-0806207
Title: DISSERTATION RESEARCH: The neuroethology of ultrasonic communication in anuran amphibians.

Among the vocal vertebrates, anuran amphibians (frogs and toads) have long been considered the champions of acoustic simplicity. However, recent research suggests that this tenet of simplicity may not always hold true. Among the most striking examples is the recent discovery of a frog species, Odorrana tormota, that communicates ultrasonically (i.e., above the upper limit of human hearing), making it the first non-mammalian vertebrate shown to communicate with extraordinarily high-frequencies. Recent recordings of the vocalizations of another frog species, Huia cavitympanum, imply that anuran ultrasonic communication is not limited to O. tormota. A subset of H. cavitympanum's high-frequency calls are entirely ultrasonic, a feature previously undocumented in amphibians. Whether they use these ultrasonic calls to communicate, however, is not yet confirmed. The objectives of the proposed research are to 1) determine whether H. cavitympanum individuals communicate ultrasonically, using both behavioral and electrophysiological techniques; 2) characterize and compare the inner ear auditory organs of H. cavitympanum and O. tormota to determine the key specializations that allow these species to hear ultrasound. This research represents an opportunity to enhance our understanding of mechanisms used by lower vertebrates, with relatively simple acoustic behavior and auditory systems, to exploit an extraordinarily high-frequency communication channel. The discovery of previously undescribed mechanisms that permit high-frequency hearing within the distinctive anuran auditory system may provide insight into the evolutionary foundations of high-frequency hearing in all vertebrate forms, including humans. In addition, because the focal species of this project, H. cavitympanum, is found only on the island of Borneo, this research presents a unique opportunity to develop relationships with Southeast Asian researchers, and to present the results of this research to a variety of cultural and socioeconomic groups. This outreach provides a scientific and social bridge between disparate cultures that can contribute to future collaboration and student exchange.

This novel finding that some Asian frogs can communicate and are sensitive to ultrasound motivates the proposed studies to examine the similarities and differences in the high-frequency/ultrasonic communication systems of the Chinese and Bornean frogs to obtain new insights into the mechanisms underlying vertebrate high-frequency communication. With the discovery of three species of frogs that communicate with ultrasonic frequencies, the field is wide open for the exploration of the mechanisms underlying ultra-high frequency transduction in a tractable vertebrate model system. Modern electrophysiological techniques will be used to examine the middle ear (tympanic membrane) and inner ear characteristics of two of the three known ultrasonically communicating frogs, and laser Doppler vibrometry will pinpoint the mechanisms for ultrasound production in these animals. This work will likely provide important new insights into the electrical and mechanical processes that underlie high-frequency tuning properties of the vertebrate auditory periphery. The unexpected ultrasonic sensitivity in anuran amphibians illustrates the remarkable adaptability of the auditory system and the extent to which evolution can modify a sensory system to adapt to its environment. Moreover, interest in these species in China and Borneo has already begun to promote long-term conservation of the habitats of these extraordinary animals. The results of this project will provide essential information on amphibian auditory physiology which will be of broad interest to conservation biologists project and would be incorporated into public outreach lectures through the Los Angeles County Museum.

The proposed experiments will test four clear hypotheses: 1: The middle and inner ears of the ultrasonic frogs exhibit adaptations for the detection of high frequencies. DPOAE measurements and laser Doppler vibrometry will be utilized to characterize in detail the auditory periphery of Odorrana- a Chinese frog which has been shown to produce and detect ultrasounds. 2: A quantitative test of the hypothesis that the DPOAE is present in the high-frequency mechanical input to the hair cell bundle in the amphibian papilla and the basilar papilla of the inner ear will be performed. A mechanical stimulus consisting of two tones of equal level will be introduced and the characteristics of resulting hair bundle motions will be investigated using a high-speed probe stimulation and imaging system. 3: The source of the ultrasonic sensitivity is the basilar papilla of the inner ear. This will be examined in two species of Asian frogs known to both produce and detect ultrasound, O. graminea and H. cavitympanum. Intracellular recordings made from ultra-high-frequency eighth nerve fibers in these frogs, followed by dye-filling and fiber tract tracing will enable the unambiguous mapping of the distal portions of these fibers to their origins in the inner ear. 4: Ultrasonic vocalization components of the frog's advertisement call are produced by the cranial portion of the medial vocal ligament (mlcr) in the larynx. The specific mechanisms used by the larynges of the frogs, O. graminea and H. cavitympanum, to produce high-frequency call elements will be investigated. The activated larynx preparation will be utilized which consists of forcing air through the larynx of euthanized males and measuring the resulting motion of at several points along the vocal folds, in addition to the mlcr, using a single-point laser Doppler vibrometer.