International audience• Stimulation of a dissected retina with a sequence of periodic dark flashes. • Extracellular spike recordings. 2. Identification of necessary components via pharmacological inhibition of synaptic transmission onto : • ON bipolar cells via mGluR6 receptor antagonist LAP-4. • OFF bipolar cells via AMPA receptor antagonist ACET. Results ON BC inhibition cancels the OSR

Buffet, Thomas

Cessac, Bruno

Ebert, Simone

Marre, Olivier

Sermet, Semichan

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The Role of Dynamical Synapses in Retinal Surprise Coding

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HAL Id: hal-03521415https://hal.inria.fr/hal-03521415Submitted on 17 Jun 2022HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoirespublics ou privés.The Role of Dynamical Synapses in Retinal SurpriseCodingSimone Ebert, Semichan Sermet, Thomas Buffet, Olivier Marre, Bruno CessacTo cite this version:Simone Ebert, Semichan Sermet, Thomas Buffet, Olivier Marre, Bruno Cessac. The Role of DynamicalSynapses in Retinal Surprise Coding. MOMI2021: Le Monde des Mathematiques Industrielles, Mar2021, Virtual, France. ￿hal-03521415￿1. Microelectrode Array Recordings:• Stimulation of a dissected retina with a sequence of periodic dark flashes.• Extracellular spike recordings. 2. Identification of necessary components  via pharmacological inhibition of synaptic transmission onto : • ON bipolar cells via mGluR6 receptor antagonist LAP-4.• OFF  bipolar cells via AMPA receptor antagonist ACET. ResultsON BC inhibition cancels the OSR.• The ON pathway is required  for the OSR to dark flashes whereas the OFF pathway is not directly required, but could still be activated by lateral input • This asymmetric contribution of ON and OFF pathway could be caused by : The Retina can recognize patterns and signal its ’surprise’  when these patterns are violated, with a high level of precision.How can a local circuit  perform such complex computations to detect ’surprise’ and which cellular mechanisms enable these computations ?We combine electrophysiological experiments in which we pharmacologically inactivate  specific cell types in the retina, to identity key components of a dynamic response to changes, withcomputational modelling to investigate the potential role and location  of short-term plasticity.MotivationExperiments23OFF BC inhibition has no direct effect on the OSR.MethodologyA) a  network effect via directed lateral     connections (amacrine cells),  B)  an intrinsic mechanism specific to ON bipolar cells. *ConclusionsThe Role of Dynamical Synapses in Retinal Surprise Coding  Simone Ebert1, Semihchan Sermet2, Thomas Buffet2, Olivier Marre2, Bruno Cessac11 Université Côte d’Azur, Inria Sophia Antipolis, France, Biovision team and Neuromod Institute2 Institut de la Vision, Sorbonne Université, Inserm S968, CNRS UMR7210, 17 Rue Moreau, 75011This work is funded by the Neuromod Institute at  Université Cote d’Azur. All experiments were performed in the team of Olivier Marre at Institut de la Vision.   • The Retina transforms visual information into spike trains transmitted to the rest of the brain. • It processes information in parallelpathways selectively responding to specific features of the visual input:• The retina also contains predictions of its future input and detects violations of its expectation with high precision. • An example of this ‘surprise signal ’ is theOmitted Stimulus Response (box 1). 1. Greg Schwartz, Rob Harris, David Shrom, and Michael J Berry. Detection and prediction of periodic patterns by the retina. Nature Neuroscience, 10 (5) : 552–554, May 2007. 2. Kastner DB, Ozuysal Y, Panagiotakos G, Baccus SA. Adaptation of Inhibition Mediates Retinal Sensitization. Curr Biol. 2019 Aug 19;29(16):2640-2651.e4 3. Baden, T., Euler, T. & Berens, P. Understanding the retinal basis of vision across species.Nat Rev Neurosci 21, 5–20 (2020). 4. Juan Gao, Greg Schwartz, Michael J. Berry II & Philip Holmes (2009) An oscillatory circuit underlying the detection of disruptions in temporally-periodic patterns, Network: Computation in Neural Systems, 20:2, 106-135,ReerencesProcessing Steps: • Step 1: Convolution of  stimulus and  a temporal kernel simulates the integration of the stimulus into bipolar cell voltage.• Step 2:  Applying a nonlinearity simulates rectification within bipolar cells.• Step 3: Kinetics of synaptic vesicle release are simulated as a dynamical system of Markov type (box 2).• Step 4:  Summation and second nonlinearity simulates transformation of the response into a ganglion cell  output firing rate .Kastner et al., 2017, Current BiologyBackground1 Modeling surprise coding in the Retina4Perspectives5Acknowledgements6References6• Synaptic vesicles can occupy  1 out of  4 different States : • P = (PR  PA  PI1 PI2 ) are probabilities to occupy each state  pulse of activity signaling the missing stimulus Peak time adapts to frequency of the presented flash sequence• Two parallel pathways that together provide input to one ganglion cell,• Directed  lateral connection before summation,• Short-term plasticity in bipolar cell and amacrine cell synapses.• The ON pathway responds to bright light,• The OFF pathway responds to dark stimuli.Can the predictive latency of the OSR be explained via the model of  STP ?Can a similar mechanism, embedded in a large scale network account for more complex patternrecognition, such as motion reversal ?We aim to build new hypothesis at the limits of biological experiments & understand computational paradigms at work. *Linear-Nonlinear-Kinetic (LNK) Model Existing Models• Existing Models explained the OSR via two antagonistic (ON-OFF) parallel pathways and  a resonance mechanism in ON bipolar cells;• This mechanism could not  be experimentally verified and cannot account fully for the predictive timing to flash frequency (box 1).  Box 2: Short-term plasticity (STP)periodic flash sequenceomitted flash*We will test a model of synaptic adaptation in silico to explore the hypothesis that dynamical synapses cause the rapid frequency adaptation. Box 1: Omitted Stimulus Response (OSR)Gao et al., 2007, Computation in Neural SystemsR :  readily releasableA :  active (released)I1 : inactive (empty)I2 : inactive (refilled)The change in probability is described by a set of  first-orderdifferential equations The output of the synapse will bedetermined by the probability of the active state, PA(t)• Transitions between states are controlled by rate constants: • fixed or vary in time, scaled by bipolar cell voltage u(t) (1). ka :  vesicle activationkfi, ksi :  fast/slow inactivationkfr,ksr : fast/slow recoveryIn future we will experimentally test if:• A lateral amacrine connection is involved in the OSR • The OFF pathway contributes indirectly to the OSRmodified from 3(1)simone.ebert@inria.fr

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The Role of Dynamical Synapses in Retinal Surprise Coding

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