Abstract

Metabolic energy can be used as a unifying principle to control neuronal activity. However, whether and how metabolic energy alone can determine the outcome of synaptic plasticity remains unclear. This study proposes a computational model of synaptic plasticity that is completely determined by energy. A simple quantitative relationship between synaptic plasticity and postsynaptic potential energy is established. Synaptic weight is directly proportional to the difference between the baseline potential energy and the suprathreshold potential energy and is constrained by the maximum energy supply. Results show that the energy constraint improves the performance of synaptic plasticity and avoids setting the hard boundary of synaptic weights. With the same set of model parameters, our model can reproduce several classical experiments in homo- and heterosynaptic plasticity. The proposed model can explain the interaction mechanism of Hebbian and homeostatic plasticity at the cellular level. Homeostatic synaptic plasticity at different time scales coexists. Homeostatic plasticity operating on a long time scale is caused by heterosynaptic plasticity and, on the same time scale as Hebbian synaptic plasticity, is caused by the constraint of energy supply.

Highlights

  • The brain accounts for only 2% of body mass, it consumes 20% of the resting metabolic energy produced by the whole body (Attwell and Laughlin, 2001; Harris et al, 2012)

  • Our model uses postsynaptic potential energy to express the change in synaptic weights

  • We presented a computational model of synaptic plasticity completely determined by energy and established a simple quantitative relationship between synaptic plasticity and postsynaptic potential energy

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Summary

Introduction

The brain accounts for only 2% of body mass, it consumes 20% of the resting metabolic energy produced by the whole body (Attwell and Laughlin, 2001; Harris et al, 2012). Maintaining resting membrane potential (15%), firing action potentials (16%), and synaptic transmission (44%) compose the energetically most expensive processes (Harris et al, 2012; Howarth et al, 2012). The majority of energy used by neurons is locally consumed at the synapse. In addition to the energetic costs of neural computation and transmission, experimental evidence indicates that synaptic plasticity is metabolically demanding (Mery and Kawecki, 2005; Jaumann et al, 2013; Placais and Preat, 2013; Placais et al, 2017). The quantitative relationship between the changes in synaptic weights (potentiation or depression) and energy consumption remains unclear

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