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J Neurosci. 2017 Jun 28;37(26):6299-6313. doi: 10.1523/JNEUROSCI.2878-16.2017. Epub 2017 May 25.

Enlargement of Ribbons in Zebrafish Hair Cells Increases Calcium Currents But Disrupts Afferent Spontaneous Activity and Timing of Stimulus Onset.

Author information

1
Department of Otolaryngology, Harvard Medical School, Boston, Massachusetts 02115.
2
Eaton-Peabody Laboratory, Massachusetts Eye and Ear, Boston, Massachusetts 02114.
3
Section on Sensory Cell Development and Function, National Institute on Deafness and Other Communication Disorders/National Institutes of Health, Bethesda, Maryland 20892.
4
Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, United Kingdom, and.
5
Advanced Imaging Core, National Institute on Deafness and Other Communication Disorders/National Institutes of Health, Bethesda, Maryland 20892.
6
Oregon Hearing Research Center and Vollum Institute, Oregon Health and Science University, Portland, Oregon 97239.
7
Department of Biology and Neuroscience Program, Amherst College, Amherst, Massachusetts 01002.
8
Section on Sensory Cell Development and Function, National Institute on Deafness and Other Communication Disorders/National Institutes of Health, Bethesda, Maryland 20892, katie.kindt@nih.gov.

Abstract

In sensory hair cells of auditory and vestibular organs, the ribbon synapse is required for the precise encoding of a wide range of complex stimuli. Hair cells have a unique presynaptic structure, the synaptic ribbon, which organizes both synaptic vesicles and calcium channels at the active zone. Previous work has shown that hair-cell ribbon size is correlated with differences in postsynaptic activity. However, additional variability in postsynapse size presents a challenge to determining the specific role of ribbon size in sensory encoding. To selectively assess the impact of ribbon size on synapse function, we examined hair cells in transgenic zebrafish that have enlarged ribbons, without postsynaptic alterations. Morphologically, we found that enlarged ribbons had more associated vesicles and reduced presynaptic calcium-channel clustering. Functionally, hair cells with enlarged ribbons had larger global and ribbon-localized calcium currents. Afferent neuron recordings revealed that hair cells with enlarged ribbons resulted in reduced spontaneous spike rates. Additionally, despite larger presynaptic calcium signals, we observed fewer evoked spikes with longer latencies from stimulus onset. Together, our work indicates that hair-cell ribbon size influences the spontaneous spiking and the precise encoding of stimulus onset in afferent neurons.SIGNIFICANCE STATEMENT Numerous studies support that hair-cell ribbon size corresponds with functional sensitivity differences in afferent neurons and, in the case of inner hair cells of the cochlea, vulnerability to damage from noise trauma. Yet it is unclear whether ribbon size directly influences sensory encoding. Our study reveals that ribbon enlargement results in increased ribbon-localized calcium signals, yet reduces afferent spontaneous activity and disrupts the timing of stimulus onset, a distinct aspect of auditory and vestibular encoding. These observations suggest that varying ribbon size alone can influence sensory encoding, and give further insight into how hair cells transduce signals that cover a wide dynamic range of stimuli.

KEYWORDS:

calcium channels; hair cell; ribbon synapse; sensory; synapse; zebrafish

PMID:
28546313
PMCID:
PMC5490065
DOI:
10.1523/JNEUROSCI.2878-16.2017
[Indexed for MEDLINE]
Free PMC Article

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