Cost of auditory sharpness: Model-Based estimate of energy use by auditory brainstem “octopus” neurons

•Temporally precise auditory brainstem ‘octopus’ cells are higly energy consuming.•This is due to a high hyperpolarization-activated mixed cation conductance.•Action potential generation in the cells costs a relatively low amount of energy.•The energy usage of individual cells can impose a constraint on their numbers. Octopus cells (OCs) of the mammalian auditory brainstem precisely encode timing of fast transient sounds and tone onsets. Sharp temporal fidelity of OCs relies on low resting membrane resistance, which suggests high energy expenditure on maintaining ion gradients across plasma membrane. We provide a model-based estimate of energy consumption in resting and spiking OCs. Our results predict that a resting OC consumes up to 2.6 × 109 ATP molecules (ATPs) per second which remarkably exceeds energy consumption of other CNS neurons. Glucose usage by all OCs in the rat is nevertheless low due to their low number. Major part of the OCs energy use results from the ion mechanisms providing for the low membrane resistance: hyperpolarization-activated mixed cation conductance and low-voltage activated K+-conductance. Spatially ordered synapses—a feature of the OCs allowing them to compensate for asynchrony of the synaptic input—brings only a 12% energy saving to OCs excitability cost. Only 13% of total OC energy used for an AP generation (1.5 × 107 ATPs) is associated with the AP generation in the axon initial segment, 64%—with synaptic currents processing and 23%—with keeping resting potential.