Sensory adaptation at ribbon synapses in the zebrafish lateral line

The 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.

Adaptation 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.