Abstract
Many sensory systems use ribbon-type synapses to transmit their signals to downstream circuits. The properties of this synaptic transfer fundamentally dictate which aspects in the original stimulus will be accentuated or suppressed, thereby partially defining the detection limits of the circuit. Accordingly, sensory neurons have evolved a wide variety of ribbon geometries and vesicle pool properties to best support their diverse functional requirements. However, the need for diverse synaptic functions does not only arise across neuron types, but also within. Here we show that UV-cones, a single type of photoreceptor of the larval zebrafish eye, exhibit striking differences in their synaptic ultrastructure and consequent calcium to glutamate transfer function depending on their location in the eye. We arrive at this conclusion by combining serial section electron microscopy and simultaneous 'dual-colour' two-photon imaging of calcium and glutamate signals from the same synapse in vivo. We further use the functional dataset to fit a cascade-like model of the ribbon synapse with different vesicle pool sizes, transfer rates, and other synaptic properties. Exploiting recent developments in simulation-based inference, we obtain full posterior estimates for the parameters and compare these across different retinal regions. The model enables us to extrapolate to new stimuli and to systematically investigate different response behaviours of various ribbon configurations. We also provide an interactive, easy-to-use version of this model as an online tool. Overall, we show that already on the synaptic level of single-neuron types there exist highly specialised mechanisms which are advantageous for the encoding of different visual features.
Highlights
Ribbon-type synapses feed high-bandwidth sensory signals into their postsynaptic networks
To establish possible structural differences amongst larval zebrafish UV-cone ribbon synapses, we obtained volumetric electron microscopy datasets of the outer retina taken from three different regions:, Acute zone (AZ), nasal (N), and dorsal (D)
Further away from the ribbon, the vesicle density was lowest in dorsal UV-cones and highest in acute zone (AZ) UV-cones (Figure 1h, Figure 1—figure supplement 1)
Summary
Ribbon-type synapses feed high-bandwidth sensory signals into their postsynaptic networks (reviewed in, e.g. Moser et al, 2020; Sterling and Matthews, 2005). Auditory systems typically operate at higher frequencies than visual systems, and auditory inner hair cells tend to use ‘faster’ ribbon synapses compared to those of photoreceptors (Baden et al, 2013a; Moser et al, 2020). Amongst photoreceptors of the vertebrate eye, rods and cones tend to differ greatly in the way they use their ribbons (Regus-Leidig and Brandstatter, 2012; Sterling and Matthews, 2005). Cones usually use multiple smaller ribbons, often positioned at different release sites in a single pedicle, to serve diverse postsynaptic circuits
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