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Diurnal modulation of multivesicular release controls the efficiency of information transmission at a sensory synapse

José Moya-Díaz, Ben James, Federico Esposti, Jamie Johnston, Leon Lagnado
doi: https://doi.org/10.1101/2021.09.12.459944
José Moya-Díaz
Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
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Ben James
Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
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Federico Esposti
Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
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Jamie Johnston
Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
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Leon Lagnado
Sussex Neuroscience, School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
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  • For correspondence: l.lagnado@sussex.ac.uk
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Summary

Sensory circuits adapt to changes in the external world or the animal’s internal state through the actions of neuromodulators1,2. Synapses are key sites at which neuromodulators act3,4 but it is not known how they alter the amount of information transmitted5. We investigated this question in the context of the diurnal regulation of visual processing in larval zebrafish, focusing on ribbon-type synapses of retinal bipolar cells6. We demonstrate that contrast-sensitivity peaks in the afternoon accompanied by an average four-fold increase in the Shannon information transmitted at individual active zones. This increase reflects higher synaptic gain, lower spontaneous “noise”, reduced variability of stimulus-evoked release and improved temporal precision. Simultaneously, an increase in the probability of multivesicular events with larger information content increases the efficiency of information transmission (bits per vesicle) by factors of 2-3. The neuromodulator dopamine contributes to all these changes in synaptic function, although ON and OFF visual channels are differentially affected. Multivesicular release is a property of synapses in many parts of the brain7-11 and this study demonstrates that it’s potentiation by neuromodulators can both increase the amount of information that is transmitted and the efficiency of transmission, revealing a previously unknown mechanism for adjusting neural processing.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted September 14, 2021.
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Diurnal modulation of multivesicular release controls the efficiency of information transmission at a sensory synapse
José Moya-Díaz, Ben James, Federico Esposti, Jamie Johnston, Leon Lagnado
bioRxiv 2021.09.12.459944; doi: https://doi.org/10.1101/2021.09.12.459944
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Diurnal modulation of multivesicular release controls the efficiency of information transmission at a sensory synapse
José Moya-Díaz, Ben James, Federico Esposti, Jamie Johnston, Leon Lagnado
bioRxiv 2021.09.12.459944; doi: https://doi.org/10.1101/2021.09.12.459944

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