Student Theses and Dissertations

Date of Award


Document Type


Degree Name

Doctor of Philosophy (PhD)

RU Laboratory

Hudspeth Laboratory


Auditory organs act as spectral analyzers by decomposing acoustic stimuli into their frequency constituents. Individual auditory afferent neurons of the VIIIth cranial nerve respond best to a particular frequency of stimulation, and are thus frequency-tuned. Much of the tuning in the inner ears of mammals is ascribed to the frequency dependence of the traveling waves on the basilar membrane, the flexible structure that houses hair cells, the auditory receptors. However, in non-mammalian vertebrates, the basilar membrane does not conduct a traveling wave. In some animals, the membrane is absent entirely. Yet auditory fibers from these animals display comparable sharpness of tuning. Though other tuning mechanisms have been characterized in these animals, they do not account for the observed sharpness found in auditory-nerve recordings. Hence, we explored the frequency response of the hair cell’s synapse in the bullfrog’s amphibian papilla, an auditory organ that lacks a basilar membrane. We monitored the synaptic output of hair cells by measuring changes in their membrane capacitance in response to sinusoidal electrical stimulation. Using perforated-patch recordings, we found that individual hair cells display frequency selectivity in synaptic exocytosis over the range of frequencies sensed by the organ. Moreover, this tuning varies from cell to cell in accordance with the cells’ tonotopic position. Using confocal imaging, we determined that hair cells tuned to high frequencies have a greater expression of the Ca 2+ buffers parvalbumin 3 and calbindin-D28k than those tuned to low frequencies. We then used an extension of an existing model for synaptic release to explore how this gradient might influence the frequency response of the synapse. Increasing buffer concentration in the absence of other changes quenches free Ca 2+ and thereby reduces the synaptic output. However, adjusting just one other release rate in conjunction could keep the system poised near a Hopf bifurcation, thereby keeping the system tuned with exquisite sensitivity to small stimuli at a particular frequency. Furthermore, the frequency range afforded by the model matched the hearing range of the organ. Thus, hair cells of the bullfrog’s amphibian papilla use synaptic tuning as an additional mechanism by which to sharpen their frequency selectivity, and a conspicuous gradient in Ca 2+ buffering may help to keep the system poised near maximal sensitivity.


A Thesis Presented to the Faculty of The Rockefeller University in Partial Fulfillment of the Requirements for the degree of Doctor of Philosophy

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