Signatures of Bayesian inference emerge from energy-efficient synapses

James Malkin, Cian O'Donnell, Conor J Houghton, Laurence Aitchison, Peter Latham (Editor), Floris P de Lange

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Abstract

Biological synaptic transmission is unreliable, and this unreliability likely degrades neural circuit performance. While there are biophysical mechanisms that can increase reliability, for instance by increasing vesicle release probability, these mechanisms cost energy. We examined four such mechanisms along with the associated scaling of the energetic costs. We then embedded these energetic costs for reliability in artificial neural networks (ANNs) with trainable stochastic synapses, and trained these networks on standard image classification tasks. The resulting networks revealed a tradeoff between circuit performance and the energetic cost of synaptic reliability. Additionally, the optimised networks exhibited two testable predictions consistent with pre-existing experimental data. Specifically, synapses with lower variability tended to have (1) higher input firing rates and (2) lower learning rates. Surprisingly, these predictions also arise when synapse statistics are inferred through Bayesian inference. Indeed, we were able to find a formal, theoretical link between the performance-reliability cost tradeoff and Bayesian inference. This connection suggests two incompatible possibilities: evolution may have chanced upon a scheme for implementing Bayesian inference by optimising energy efficiency, or alternatively, energy-efficient synapses may display signatures of Bayesian inference without actually using Bayes to reason about uncertainty.
Original languageEnglish
Article numberRP92595
JournaleLife
Volume12
Early online date6 Aug 2024
DOIs
Publication statusPublished online - 6 Aug 2024

Bibliographical note

Publisher Copyright:
© 2023, Malkin et al.

Data Access Statement

The current manuscript is a computational study, so any data generated is simulated data. The previously published dataset listed below and data from Ko et al., 2013 were used. All newly generated
data is available at: https://github.com/JamesMalkin/EfficientBayes, copy archived at Malkin, 2024.

The following previously published dataset was used:
Author(s) Year Dataset title Dataset URL Database and Identifier
Costa R, Froemke
R, Sjöström P, van
Rossum M
2015 Data from: Unified pre- and
postsynaptic long-term
plasticity enables reliable
and flexible learning
https://doi.org/10.
5061/dryad.p286g
Dryad Digital Repository,
10.5061/dryad.p286g

Keywords

  • synaptic plasticity
  • Bayesian inference
  • energy efficiency
  • computational neuroscience
  • None
  • neuroscience
  • none

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