Presynaptic stochasticity improves energy efficiency and helps alleviate the stability-plasticity dilemma

  1. Simon Schug  Is a corresponding author
  2. Frederik Benzing
  3. Angelika Steger
  1. University of Zurich and ETH Zurich, Switzerland
  2. ETH Zurich, Switzerland

Abstract

When an action potential arrives at a synapse there is a large probability that no neurotransmitter is released. Surprisingly, simple computational models suggest that these synaptic failures enable information processing at lower metabolic costs. However, these models only consider information transmission at single synapses ignoring the remainder of the neural network as well as its overall computational goal. Here, we investigate how synaptic failures affect the energy efficiency of models of entire neural networks that solve a goal-driven task. We find that presynaptic stochasticity and plasticity improve energy efficiency and show that the network allocates most energy to a sparse subset of important synapses. We demonstrate that stabilising these synapses helps to alleviate the stability-plasticity dilemma, thus connecting a presynaptic notion of importance to a computational role in lifelong learning. Overall, our findings present a set of hypotheses for how presynaptic plasticity and stochasticity contribute to sparsity, energy efficiency and improved trade-offs in the stability-plasticity dilemma.

Data availability

Code for experiments is part of the submission and is published on GitHub (https://github.com/smonsays/presynaptic-stochasticity).

The following previously published data sets were used

Article and author information

Author details

  1. Simon Schug

    Institute of Neuroinformatics,, University of Zurich and ETH Zurich, Zurich, Switzerland
    For correspondence
    sschug@ethz.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5305-2547
  2. Frederik Benzing

    Department of Computer Science, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Angelika Steger

    Department of Computer Science, ETH Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

Funding

Swiss National Science Foundation (Ambizione Grant,PZ00P318602)

  • Simon Schug

Swiss National Science Foundation (CRSII5_173721)

  • Frederik Benzing
  • Angelika Steger

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2021, Schug et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,097
    views
  • 215
    downloads
  • 17
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Simon Schug
  2. Frederik Benzing
  3. Angelika Steger
(2021)
Presynaptic stochasticity improves energy efficiency and helps alleviate the stability-plasticity dilemma
eLife 10:e69884.
https://doi.org/10.7554/eLife.69884

Share this article

https://doi.org/10.7554/eLife.69884

Further reading

    1. Neuroscience
    David C Williams, Amanda Chu ... Michael A McDannald
    Research Advance

    Recognizing and responding to threat cues is essential to survival. Freezing is a predominant threat behavior in rats. We have recently shown that a threat cue can organize diverse behaviors beyond freezing, including locomotion (Chu et al., 2024). However, that experimental design was complex, required many sessions, and had rats receive many foot shock presentations. Moreover, the findings were descriptive. Here, we gave female and male Long Evans rats cue light illumination paired or unpaired with foot shock (8 total) in a conditioned suppression setting, using a range of shock intensities (0.15, 0.25, 0.35, or 0.50 mA). We found that conditioned suppression was only observed at higher foot shock intensities (0.35 mA and 0.50 mA). We constructed comprehensive temporal ethograms by scoring 22,272 frames across 12 behavior categories in 200-ms intervals around cue light illumination. The 0.50 mA and 0.35 mA shock-paired visual cues suppressed reward seeking, rearing, and scaling, as well as light-directed rearing and light-directed scaling. The shock-paired visual cue further elicited locomotion and freezing. Linear discriminant analyses showed that ethogram data could accurately classify rats into paired and unpaired groups. Using complete ethogram data produced superior classification compared to behavior subsets, including an Immobility subset featuring freezing. The results demonstrate diverse threat behaviors – in a short and simple procedure – containing sufficient information to distinguish the visual fear conditioning status of individual rats.

    1. Neuroscience
    Agnieszka Glica, Katarzyna Wasilewska ... Katarzyna Jednoróg
    Research Article

    The neural noise hypothesis of dyslexia posits an imbalance between excitatory and inhibitory (E/I) brain activity as an underlying mechanism of reading difficulties. This study provides the first direct test of this hypothesis using both electroencephalography (EEG) power spectrum measures in 120 Polish adolescents and young adults (60 with dyslexia, 60 controls) and glutamate (Glu) and gamma-aminobutyric acid (GABA) concentrations from magnetic resonance spectroscopy (MRS) at 7T MRI scanner in half of the sample. Our results, supported by Bayesian statistics, show no evidence of E/I balance differences between groups, challenging the hypothesis that cortical hyperexcitability underlies dyslexia. These findings suggest that alternative mechanisms must be explored and highlight the need for further research into the E/I balance and its role in neurodevelopmental disorders.