Distinct synaptic transfer functions in same-type photoreceptors

Schroeder, Cornelius, Oesterle, Jonathan, Berens, Philipp, Yoshimatsu, Takeshi and Baden, Tom (2021) Distinct synaptic transfer functions in same-type photoreceptors. Elife, 10. a67851 1-24. ISSN 2050-084X

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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.

Item Type: Article
Keywords: neuroscience, zebrafish
Schools and Departments: School of Life Sciences > Neuroscience
SWORD Depositor: Mx Elements Account
Depositing User: Mx Elements Account
Date Deposited: 04 Aug 2021 08:02
Last Modified: 01 Mar 2022 10:34
URI: http://sro.sussex.ac.uk/id/eprint/100915

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Project NameSussex Project NumberFunderFunder Ref
Anisotropic retinal circuits for processing of colour and space in natureG2397BBSRC-BIOTECHNOLOGY & BIOLOGICAL SCIENCES RESEARCH COUNCILBB/R014817/1
Anisotropic retinal circuits for processing of colour and space in nature - Lister Institute Research PrizeG2503LISTER INSTITUTEUnset
How to connect an eye to a brainG3137WELLCOME TRUSTWT Ref: 220277/
NeuroVisEco - Zebrafish vision in its natural context: from natural scenes through retinal and central processing to behaviourG1871EUROPEAN UNION677687
Philip Leverhulme Prize - Biological SciencesG2276LEVERHULME TRUSTPLP-2017-005