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Enrichment and differential targeting of complexins 3 and 4 in ribbon-containing sensory neurons during zebrafish development.

ABSTRACT: BACKGROUND:In sensory systems with broad bandwidths, polarized receptor cells utilize highly specialized organelles in their apical and basolateral compartments to transduce and ultimately transmit signals to the rest of the nervous system. While progress has been made in elucidating the assembly of the transduction apparatus, the development of synaptic ribbon-containing terminals remains poorly understood. To begin to delineate the targeting of the exocytotic machinery specifically in ribbon-containing neurons, we have examined the expression of complexins 3 and 4 in the zebrafish visual and acousticolateral systems during the first week of development. RESULTS:We have identified five members of the complexin 3/4 subfamily in zebrafish that show 50 to 75% amino acid identity with mammalian complexins 3 and 4. Utilizing a polyclonal antibody that recognizes all five orthologs, we demonstrate that these proteins are enriched in ribbon-containing sensory neurons. Complexin 3/4 is rapidly targeted to presynaptic terminals in the pineal organ and retina concomitantly with RIBEYE b, a component of ribbons. In hair cells of the inner ear and lateral line, however, complexin 3/4 immunoreactivity clusters on the apical surfaces of hair cells, among their stereocilia, rather than along the basolateral plasma membrane with RIBEYE b. A complexin 4a-specific antibody selectively labels the presynaptic terminals of visual system ribbon-containing neurons. CONCLUSIONS:These results provide evidence for the concurrent transport and/or assembly of multiple components of the active zone in developing ribbon terminals. Members of the complexin 3/4 subfamily are enriched in these terminals in the visual system and in hair bundles of the acousticolateral system, suggesting that these proteins are differentially targeted and may have multiple roles in ribbon-containing sensory neurons.

SUBMITTER: Zanazzi G

PROVIDER: S-EPMC2941751 | biostudies-literature | 2010 Sep

REPOSITORIES: biostudies-literature

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Enrichment and differential targeting of complexins 3 and 4 in ribbon-containing sensory neurons during zebrafish development.

Zanazzi George G Matthews Gary G

Neural development 20100901

<h4>Background</h4>In sensory systems with broad bandwidths, polarized receptor cells utilize highly specialized organelles in their apical and basolateral compartments to transduce and ultimately transmit signals to the rest of the nervous system. While progress has been made in elucidating the assembly of the transduction apparatus, the development of synaptic ribbon-containing terminals remains poorly understood. To begin to delineate the targeting of the exocytotic machinery specifically in ...[more]

PMID: 20809954

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Project description:Key pointsThe present study aimed to determine the sensory adaptation characteristics of hair cell ribbon synapses in vivo. Hair cells of the zebrafish lateral line transmit hydrodynamic stimuli to the posterior lateral line ganglion afferent neurons. Excitatory hair bundle deflections by water-jet stimuli cause glutamate release at hair cell synapses with a rapid (phasic) and a sustained component, which are likely linked to the exocytosis of distinct vesicle pools. The glutamate-induced increase in afferent neuron firing rate adapts over time, which is mirrored by the depression of neurotransmitter release, without preventing phase-locking. Adaptation also occurs during inhibitory hair bundle displacements, highlighting a shift in the sensitivity range of the lateral line during prolonged stimulation. Postsynaptic mechanisms exert some degree of regulation on the afferent firing adaptation. We conclude that vesicle depletion is the primary determinant of firing rate adaptation, allowing lateral line hair cell ribbon synapses to maintain sensitivity to sustained stimuli.AbstractAdaptation is used by sensory systems to adjust continuously their sensitivity to match changes in environmental stimuli. In the auditory and vestibular systems, the release properties of glutamate-containing vesicles at the hair cell ribbon synapses play a crucial role in sensory adaptation, thus shaping the neural response to sustained stimulation. How ribbon synapses regulate the release of glutamate and how they modulate afferent responses in vivo is still largely unknown. Here, we have used two-photon imaging and electrophysiology to investigate the synaptic transfer characteristics of the hair cells in the context of sensory adaptation in live zebrafish. Prolonged and repeated water-jet stimulation of the hair cell stereociliary bundles caused adaptation of the action potential firing rate elicited in the afferent neurons. By monitoring glutamate at ribbon synapses using time-lapse imaging, we identified two kinetically distinct release components: a rapid response that was exhausted within 50-100 ms and a slower and sustained response lasting the entire stimulation. After repeated stimulations, the recovery of the fast component followed a biphasic time course. Depression of glutamate release was largely responsible for the rapid firing rate adaptation recorded in the afferent neurons. However, postsynaptic Ca2+ responses had a slower recovery time course compared to that of glutamate release, indicating that they are likely to contribute to the afferent firing adaptation. Hair cells also exhibited a form of adaptation during inhibitory bundle stimulations. We conclude that hair cells have optimised their synaptic machinery to encode prolonged stimuli and to maintain their sensitivity to new incoming stimuli.

Dataset Information

Enrichment and differential targeting of complexins 3 and 4 in ribbon-containing sensory neurons during zebrafish development.

Publications

Enrichment and differential targeting of complexins 3 and 4 in ribbon-containing sensory neurons during zebrafish development.

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