Distinct Synaptic Transfer Functions in Same-Type Photoreceptors

Abstract

Summary. 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″ 2-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 specialized mechanisms which are advantageous for the encoding of different visual features.

A theory of synaptic transmission

“…In contrast, the present theory is applicable to a wide variety of synaptic types, despite the differences in their fusion pathways, different calcium sensors that they implement (Wolfes and Dean, 2020) and different couplings between their regulatory proteins (Kasai et al, 2012;Gramlich and Klyachko, 2019). Indeed, recent experiments have suggested that the calcium-response properties of synapses are much more diverse than had been thought previously (Özçete and Moser, 2021;Gómez-Casati and Goutman, 2021;Schroeder et al, 2021). Second, the existing models did not produce analytic expressions for the key observables that emerge from the experiments, which limits the predictive value of these models, their utility in extracting information from the experiments, and their ability to reveal the organizing principles of synaptic transmission.…”

Ancestral circuits for vertebrate color vision emerge at the first retinal synapse

“…Because the larval zebrafish eye is both structurally and functionally asymmetrical ( 11 , 14 , 25 – 28 ), we always sampled from four different regions of the eye’s sagittal plane: dorsal (D), nasal (N), ventral (V), and the area temporalis [acute zone, also known as “strike zone” ( 14 )]. With exceptions noted below (see also Discussion), we found that the spectral tuning of cones was approximately eye position invariant (fig.…”

Ancestral circuits for vertebrate colour vision emerge at the first retinal synapse

“…S1d-g) and were kept for further analysis. Because the larval zebrafish eye is both structurally and functionally asymmetrical (10,13,(24)(25)(26)(27), we always sampled from four different regions of the eye's sagittal plane: dorsal (D), nasal (N), ventral (V) and the area temporalis (acute zone, AZ (also known as "strike zone" (13))). With exceptions noted below (see also Discussion), we found that the spectral tuning of cones was approximately eye-position invariant (Fig.…”