Function and energy consumption constrain neuronal biophysics in a canonical computation

Coincidence detection

Michiel W.H. Remme, John Rinzel, Susanne Schreiber

Research output: Contribution to journalArticle

Abstract

Neural morphology and membrane properties vary greatly between cell types in the nervous system. The computations and local circuit connectivity that neurons support are thought to be the key factors constraining the cells’ biophysical properties. Nevertheless, additional constraints can be expected to further shape neuronal design. Here, we focus on a particularly energy-intense system (as indicated by metabolic markers): principal neurons in the medial superior olive (MSO) nucleus of the auditory brainstem. Based on a modeling approach, we show that a trade-off between the level of performance of a functionally relevant computation and energy consumption predicts optimal ranges for cell morphology and membrane properties. The biophysical parameters appear most strongly constrained by functional needs, while energy use is minimized as long as function can be maintained. The key factors that determine model performance and energy consumption are 1) the saturation of the synaptic conductance input and 2) the temporal resolution of the postsynaptic signals as they reach the soma, which is largely determined by active membrane properties. MSO cells seem to operate close to pareto optimality, i.e., the trade-off boundary between performance and energy consumption that is formed by the set of optimal models. Good performance for drastically lower costs could in theory be achieved by small neurons without dendrites, as seen in the avian auditory system, pointing to additional constraints for mammalian MSO cells, including their circuit connectivity.

Original languageEnglish (US)
Article numbere1006612
JournalPLoS Computational Biology
Volume14
Issue number12
DOIs
StatePublished - Dec 1 2018

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biophysics
Biophysics
Coincidence
Neurons
Energy Consumption
Energy utilization
membrane
Membranes
trade-off
connectivity
Cell
Neuron
Membrane
neurons
Networks (circuits)
Neurology
cells
nervous system
energy use
Connectivity

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Modeling and Simulation
  • Ecology
  • Molecular Biology
  • Genetics
  • Cellular and Molecular Neuroscience
  • Computational Theory and Mathematics

Cite this

Function and energy consumption constrain neuronal biophysics in a canonical computation : Coincidence detection. / Remme, Michiel W.H.; Rinzel, John; Schreiber, Susanne.

In: PLoS Computational Biology, Vol. 14, No. 12, e1006612, 01.12.2018.

Research output: Contribution to journalArticle

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