Multitask learning of a biophysically-detailed neuron model

PLoS Comput Biol. 2024 Jul 31;20(7):e1011728. doi: 10.1371/journal.pcbi.1011728. eCollection 2024 Jul.

Abstract

The human brain operates at multiple levels, from molecules to circuits, and understanding these complex processes requires integrated research efforts. Simulating biophysically-detailed neuron models is a computationally expensive but effective method for studying local neural circuits. Recent innovations have shown that artificial neural networks (ANNs) can accurately predict the behavior of these detailed models in terms of spikes, electrical potentials, and optical readouts. While these methods have the potential to accelerate large network simulations by several orders of magnitude compared to conventional differential equation based modelling, they currently only predict voltage outputs for the soma or a select few neuron compartments. Our novel approach, based on enhanced state-of-the-art architectures for multitask learning (MTL), allows for the simultaneous prediction of membrane potentials in each compartment of a neuron model, at a speed of up to two orders of magnitude faster than classical simulation methods. By predicting all membrane potentials together, our approach not only allows for comparison of model output with a wider range of experimental recordings (patch-electrode, voltage-sensitive dye imaging), it also provides the first stepping stone towards predicting local field potentials (LFPs), electroencephalogram (EEG) signals, and magnetoencephalography (MEG) signals from ANN-based simulations. While LFP and EEG are an important downstream application, the main focus of this paper lies in predicting dendritic voltages within each compartment to capture the entire electrophysiology of a biophysically-detailed neuron model. It further presents a challenging benchmark for MTL architectures due to the large amount of data involved, the presence of correlations between neighbouring compartments, and the non-Gaussian distribution of membrane potentials.

MeSH terms

  • Action Potentials / physiology
  • Brain / physiology
  • Computational Biology
  • Computer Simulation
  • Electroencephalography / methods
  • Humans
  • Machine Learning
  • Magnetoencephalography / methods
  • Membrane Potentials* / physiology
  • Models, Neurological*
  • Neural Networks, Computer*
  • Neurons* / physiology

Grants and funding

This research was funded by UiO:Life Science through the 4MENT convergence environment to JV, the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement N° 945371 to KB and the European Union Horizon 2020 Research and Innovation Programme under Grant Agreement No. 945539 Human Brain Project(HBP) SGA3 to JV. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.