Neuronal degeneracy reflects context-specific trade-offs between energy and information

Abstract

Among neurons of the same type, the different electrophysiological parameters vary drastically. It is presently unclear if there is any hidden structure in this diversity and how it relates to neuronal function. One potential source of structure is the evolutionary pressure that has sculpted brains to work in an energy-efficient manner. Here we show that neurons parameters do not vary randomly, but that neurons populate a manifold within their parameter space permitting energy-efficient signaling. This manifold represents a Pareto front of degenerate solutions to the problem of energy-efficiency and explains the prevalence of low to intermediate firing rates (2 - 5 Hz) in neocortex. Furthermore, we show that neurons in different sensory brain areas populate different manifolds and that food restriction induces systematic shifts of neuronal parameters along this manifold. Our results suggest that the large diversity of neuronal properties is actually tightly regulated to ensure energy-efficient signaling in different contexts. In briefWe show that there is hidden structure in the diversity of electrophysiological properties of neurons that is governed by trade-offs between energy consumption and information transmission. HighlightsO_LIWe derive an updated neuronal energy budget for a large class of neuron models. C_LIO_LIComputational modeling predicts a manifold of degenerate solutions to energy-efficient information coding forming a Pareto front in the neuronal parameter space. C_LIO_LINeurons from visual and somatosensory cortex fall on the predicted manifold. C_LIO_LIOptimal energy-efficiency is achieved for intermediate-low firing rates (2 - 5 Hz) as observed in neocortex. C_LIO_LIWe observe an energy-efficient form of non-multiplicative synaptic scaling during food deprivation. C_LI O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=164 SRC="FIGDIR/small/708507v2_ufig1.gif" ALT="Figure 1"> View larger version (36K): org.highwire.dtl.DTLVardef@ca6d36org.highwire.dtl.DTLVardef@1c81ca3org.highwire.dtl.DTLVardef@d03833org.highwire.dtl.DTLVardef@19bc7c_HPS_FORMAT_FIGEXP M_FIG C_FIG