Ion channel distributions in cortical neurons are optimized for energy-efficient active dendritic computations

Abstract

The mammalian brain has an enormous demand for energy, which is thought to impose strong selective pressure by which the neurons evolve in ways that ensure robust function at minimal energy cost. However, which principles drive the ion channel distributions in the dendrites to implement different neuronal functions is yet unclear. Here we found that an energy-efficient generation of dendritic calcium action potentials in cortical pyramidal neurons requires a low expression of slow inactivating potassium channels. We demonstrate that this relationship between energy cost and neuronal function is independent of the dendritic morphology and the expression patterns of other ion channels that implement additional perisomatic and dendritic functions. Moreover, we found that calcium action potentials can arise from a wide spectrum of ion channel expression patterns, including configurations with high potassium channel densities in the dendrites. These configurations can account equally well for the characteristic intrinsic physiology of the pyramidal neurons. However, only configurations with low potassium channel densities in the distal dendrites are observed empirically. Thus, our findings indicate that cortical neurons do not utilize all theoretically possible ways to implement their functions, but instead select those optimized for energy-efficient active dendritic computations.