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

Patel, Suchit H.; Salvi, Joshua D.; Maoiléidigh, Dáibhid Ó; Hudspeth, A. J.

doi:10.1523/jneurosci.1246-12.2012

Cited by 15 publications

(14 citation statements)

References 36 publications

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“…By contrast, the low Ca 2+ buffer capacity in high-frequency basal IHCs, which is required for their graded release, will make them more prone to Ca 2+ -induced cytotoxicity. A tonotopic gradient in Ca 2+ -binding protein expression has been reported in auditory hair cells ( Hackney et al, 2003 , 2005 ; Patel et al, 2012 ), which may facilitate a frequency-dependent tuning of exocytosis in some animal species ( Schnee et al, 2005 ; Rutherford and Roberts, 2006 ; Patel et al, 2012 ).…”

Section: Discussionmentioning

confidence: 98%

The Coupling between Ca²⁺Channels and the Exocytotic Ca²⁺Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

et al. 2017

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The cochlea processes auditory signals over a wide range of frequencies and intensities. However, the transfer characteristics at hair cell ribbon synapses are still poorly understood at different frequency locations along the cochlea. Using recordings from mature gerbils, we report here a surprisingly strong block of exocytosis by the slow Ca2+ buffer EGTA (10 mM) in basal hair cells tuned to high frequencies (∼30 kHz). In addition, using recordings from gerbil, mouse, and bullfrog auditory organs, we find that the spatial coupling between Ca2+ influx and exocytosis changes from nanodomain in low-frequency tuned hair cells (∼<2 kHz) to progressively more microdomain in high-frequency cells (∼>2 kHz). Hair cell synapses have thus developed remarkable frequency-dependent tuning of exocytosis: accurate low-latency encoding of onset and offset of sound intensity in the cochlea's base and submillisecond encoding of membrane receptor potential fluctuations in the apex for precise phase-locking to sound signals. We also found that synaptic vesicle pool recovery from depletion was sensitive to high concentrations of EGTA, suggesting that intracellular Ca2+ buffers play an important role in vesicle recruitment in both low- and high-frequency hair cells. In conclusion, our results indicate that microdomain coupling is important for exocytosis in high-frequency hair cells, suggesting a novel hypothesis for why these cells are more susceptible to sound-induced damage than low-frequency cells; high-frequency inner hair cells must have a low Ca2+ buffer capacity to sustain exocytosis, thus making them more prone to Ca2+-induced cytotoxicity.SIGNIFICANCE STATEMENT In the inner ear, sensory hair cells signal reception of sound. They do this by converting the sound-induced movement of their hair bundles present at the top of these cells, into an electrical current. This current depolarizes the hair cell and triggers the calcium-induced release of the neurotransmitter glutamate that activates the postsynaptic auditory fibers. The speed and precision of this process enables the brain to perceive the vital components of sound, such as frequency and intensity. We show that the coupling strength between calcium channels and the exocytosis calcium sensor at inner hair cell synapses changes along the mammalian cochlea such that the timing and/or intensity of sound is encoded with high precision.

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Section: Discussionmentioning

confidence: 98%

The Coupling between Ca²⁺Channels and the Exocytotic Ca²⁺Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

et al. 2017

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“…However, when we use sine wave stimuli of different frequencies, but fixed amplitude, the low frequency stimulus produces shorter synaptic delays than high frequency stimuli (Figure S4) and a spike phase advance (Figure 4D). Interestingly, sacculus bullfrog hair cells are tuned to release more efficiently with weak stimuli at their characteristic frequencies and this form of evoked exocytosis also appears to be Ca 2+ -current independent (Rutherford and Roberts, 2006) and is present in the amphibian papilla (Patel et al, 2012). …”

Section: Discussionmentioning

confidence: 99%

Phase-Locking Precision Is Enhanced by Multiquantal Release at an Auditory Hair Cell Ribbon Synapse

Cho

Gersdorff

2014

Neuron

115

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Sound-evoked spikes in the auditory nerve can phase-lock with submillisecond precision for prolonged periods of time. However, the synaptic mechanisms that enable this accurate spike firing remain poorly understood. Using paired recordings from adult frog hair cells and their afferent fibers we show here that during sinewave stimuli EPSC failures occur even during strong stimuli. However, exclusion of EPSC failures leads to mean EPSC amplitudes that are independent of Ca2+ current. Given the intrinsic jitter in spike triggering, evoked EPSPs and spikes had surprisingly similar degrees of synchronization to a sinewave stimulus. This similarity was explained by an unexpected finding: large-amplitude multiquantal EPSCs have a significantly larger synchronization index than smaller evoked EPSCs. Large EPSPs therefore enhance the precision of spike timing. The hair cells’ unique capacity for continuous, large-amplitude, and highly synchronous multiquantal release thus underlies its ability to trigger phase-locked spikes in afferent fibers.

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“…However, the experimental data in this study and many similar studies were collected at a location of 16–19 kHz, at which electrical tuning is unlikely to be feasible. In addition to mechanical and electrical tuning, exocytosis from hair cells is believed to be frequency‐selective (Patel et al, ; Rutherford and Roberts, ), making ribbon synapses a third source for frequency tuning in the inner ear. To untangle contributions of different tuning mechanisms, it is necessary to examine how each tuning mechanism aligns or misaligns with one another in frequency domain.…”

Section: Discussionmentioning

confidence: 99%

Probing electrical tuning of hair cells with a Zap current method in the intact amphibian papilla of bullfrogs

Frolov

2016

Synapse

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Most, if not all, modern vertebrate species have evolved exquisite inner ears to discriminate acoustic signals of different frequencies, through a process called frequency tuning. For non-mammalian species, at least part of frequency tuning has been attributed to intrinsic electrical properties of hair cells, i.e. electrical tuning. Since it was first discovered, the traditional method to assess electrical tuning has been to inject step current into hair cells and examine dampened membrane voltage oscillation. However, this method is not applicable for hair cells that do not oscillate. In this study, we developed a Zap current method that can be unbiasedly applied to all hair cells regardless of their oscillating behavior. Similar to a chirp sound in acoustic stimulation, a Zap current is a sinusoidal current with the frequency increased linearly with time. We first validated this new method with the traditional step current method on hair cells with dampened membrane voltage oscillation, and then applied it to all hair cells in the intact amphibian papilla of bullfrogs. We found that while hair cells with dampened membrane voltage oscillation are sharply tuned, non-oscillating hair cells are broadly tuned. In addition, we found a third type of hair cells, which oscillate continuously and are extremely sharply tuned, with multiple peaks that are reminiscent of harmonics in the mammalian cochlea. In conclusion, the new Zap current method provides an unbiased way to assess electrical tuning, and it reveals an underappreciated heterogeneity of electrical tuning in the bullfrog amphibian papilla.

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

Cited by 15 publications

References 36 publications

The Coupling between Ca²⁺Channels and the Exocytotic Ca²⁺Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

The Coupling between Ca²⁺Channels and the Exocytotic Ca²⁺Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

Phase-Locking Precision Is Enhanced by Multiquantal Release at an Auditory Hair Cell Ribbon Synapse

Probing electrical tuning of hair cells with a Zap current method in the intact amphibian papilla of bullfrogs

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

Cited by 15 publications

References 36 publications

The Coupling between Ca2+Channels and the Exocytotic Ca2+Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

The Coupling between Ca2+Channels and the Exocytotic Ca2+Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

Phase-Locking Precision Is Enhanced by Multiquantal Release at an Auditory Hair Cell Ribbon Synapse

Probing electrical tuning of hair cells with a Zap current method in the intact amphibian papilla of bullfrogs

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The Coupling between Ca²⁺Channels and the Exocytotic Ca²⁺Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea

The Coupling between Ca²⁺Channels and the Exocytotic Ca²⁺Sensor at Hair Cell Ribbon Synapses Varies Tonotopically along the Mature Cochlea