Exocytosis in the Frog Amphibian Papilla

Quinones, Patricia Martinez; Luu, Cindy; Schweizer, Felix E.; Narins, Peter M.

doi:10.1007/s10162-011-0304-1

Cited by 6 publications

(4 citation statements)

References 63 publications

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“…What accounts for the difference between the present findings and an earlier investigation that showed no frequency-selective exocytosis in the amphibian papilla of the grass frog (Quiñones et al, 2012)? First, the previous study pooled data from numerous cells in two large segments of the papilla, potentially obscuring sharp tuning curves.…”

Section: Discussioncontrasting

confidence: 99%

Frequency-Selective Exocytosis by Ribbon Synapses of Hair Cells in the Bullfrog's Amphibian Papilla

Patel¹,

Salvi²,

Maoiléidigh³

et al. 2012

J. Neurosci.

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The activity of auditory afferent fibers depends strongly on the frequency of stimulation. Although the bullfrog's amphibian papilla lacks the flexible basilar membrane that effects tuning in mammals, its afferents display comparable frequency selectivity. Seeking additional mechanisms of tuning in this organ, we monitored the synaptic output of hair cells by measuring changes in their membrane capacitance during sinusoidal electrical stimulation at various frequencies. Using perforated-patch recordings, we found that individual hair cells displayed frequency selectivity in synaptic exocytosis within the frequency range sensed by the amphibian papilla. Moreover, each cell's tuning varied in accordance with its tonotopic position. Using confocal imaging, we observed a tonotopic gradient in the concentration of proteinaceous Ca2+ buffers. A model for synaptic release suggests that this gradient maintains the sharpness of tuning. We conclude that hair cells of the amphibian papilla use synaptic tuning as an additional mechanism for sharpening their frequency selectivity.

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Section: Discussioncontrasting

confidence: 99%

Frequency-Selective Exocytosis by Ribbon Synapses of Hair Cells in the Bullfrog's Amphibian Papilla

Patel¹,

Salvi²,

Maoiléidigh³

et al. 2012

J. Neurosci.

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“…We also observed an increase in exocytosis efficiency, which indicates the exocytosis increase is not proportional to the increase of Ca 2ϩ current. A nonlinear power law dependence of exocytosis on free Ca 2ϩ ion concentration could potentially explain our results of a high Q 10 ϭ 2.4 for exocytosis elicited by 20 ms depolarizing pulses (Cho and von Gersdorff, 2012;Quiñones et al, 2012). However, a linear dependence of exocytosis on Ca 2ϩ current charge has been found for mid-frequency tuned bullfrog hair cells (Keen and Hudspeth, 2006;Cho et al, 2011).…”

Section: Electrical Resonance At High Temperaturementioning

confidence: 61%

How to Build a Fast and Highly Sensitive Sound Detector That Remains Robust to Temperature Shifts

Chen

Gersdorff

2019

J. Neurosci.

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Frogs must have sharp hearing abilities during the warm summer months to successfully find mating partners. This study aims to understand how frog hair cell ribbon-type synapses preserve both sensitivity and temporal precision during temperature changes. Under room (ϳ24°C) and high (ϳ32°C) temperature, we performed in vitro patch-clamp recordings of hair cells and their afferent fibers in amphibian papillae of either male or female bullfrogs. Afferent fibers exhibited a wide heterogeneity in membrane input resistance (R in ) from 100 M⍀ to 1000 M⍀, which may contribute to variations in spike threshold and firing frequency. At higher temperatures, most fibers increased their frequency of spike firing due to an increase in spontaneous EPSC frequencies. Hair cell resting membrane potential (V rest ) remained surprisingly stable during temperature increases, because Ca 2ϩ influx and K ϩ outflux increased simultaneously. This increase in Ca 2ϩ current likely enhanced spontaneous EPSC frequencies. These larger "leak currents" at V rest also lowered R in and produced higher electrical resonant frequencies. Lowering R in will reduce the hair cells receptor potential and presumably moderate the systems sensitivity. Using membrane capacitance measurements, we suggest that hair cells can partially compensate for this reduced sensitivity by increasing exocytosis efficiency and the size of the readily releasable pool of synaptic vesicles. Furthermore, paired recordings of hair cells and their afferent fibers showed that synaptic delays shortened and multivesicular release becomes more synchronous at higher temperatures, which should improve temporal precision. Together, our results explain many previous in vivo observations on the temperature dependence of spikes in auditory nerves.

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“…Moreover, otoferlin alone cannot account for the high-order to linear change in Ca 2+ sensitivity of exocytosis upon functional maturation [ 7 ], nor for exocytosis that occurs in early postnatal IHCs [ 31 ]. Instead, Syt-4, a unique but ubiquitous isoform of synaptotagmin that does not bind calcium in the C 2 A Ca 2+ -sensing domain [ 33 ], is an essential element for the linear exocytotic Ca 2+ dependence in IHCs [ 7 , 38 ] and exocytosis in hair cells from lower vertebrates [ 40 ]. The direct involvement of Syt-4 in hair cell exocytosis is further supported by the fact that, unlike Syt-2 (see below), it does not act as a modulator of IHC development through either the activity of the efferent system (see Results above) or the auditory afferents (as a retrograde regulator released by the afferent auditory fibres [ 7 ].…”

Section: Discussionmentioning

confidence: 99%

Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses

et al. 2013

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Spontaneous electrical activity generated by developing sensory cells and neurons is crucial for the maturation of neural circuits. The full maturation of mammalian auditory inner hair cells (IHCs) depends on patterns of spontaneous action potentials during a ‘critical period’ of development. The intrinsic spiking activity of IHCs can be modulated by inhibitory input from cholinergic efferent fibres descending from the brainstem, which transiently innervate immature IHCs. However, it remains unknown whether this transient efferent input to developing IHCs is required for their functional maturation. We used a mouse model that lacks the α9-nicotinic acetylcholine receptor subunit (α9nAChR) in IHCs and another lacking synaptotagmin-2 in the efferent terminals to remove or reduce efferent input to IHCs, respectively. We found that the efferent system is required for the developmental linearization of the Ca2+-sensitivity of vesicle fusion at IHC ribbon synapses, without affecting their general cell development. This provides the first direct evidence that the efferent system, by modulating IHC electrical activity, is required for the maturation of the IHC synaptic machinery. The central control of sensory cell development is unique among sensory systems.

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Exocytosis in the Frog Amphibian Papilla

Cited by 6 publications

References 63 publications

Frequency-Selective Exocytosis by Ribbon Synapses of Hair Cells in the Bullfrog's Amphibian Papilla

Frequency-Selective Exocytosis by Ribbon Synapses of Hair Cells in the Bullfrog's Amphibian Papilla

How to Build a Fast and Highly Sensitive Sound Detector That Remains Robust to Temperature Shifts

Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses

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