Differential energetic profile of signal processing in central vestibular neurons.

Background: Energetic aspects of neuronal activity have become a major focus of interest given the fact that the brain among all organs dominates the oxygen consumption. At variance with the importance of neuroenergetics, the knowledge about how electrical activity and metabolism is correlated in defined neuronal populations is still rather scarce.

Results: We have estimated the ATP consumption in the two physiologically well characterized populations of frog central vestibular neurons, with tonic and phasic firing patterns, respectively. These two distinct groups of neurons jointly process head/body movements detected by semicircular canal and otolith organs in the inner ear. The ATP consumption for maintenance of the resting membrane potential (V) and postsynaptic action potential (AP) generation was calculated based on the wealth of previously reported morpho-physiological features of these two neuronal types. Accordingly, tonic vestibular neurons require less ATP across the physiological activity range for these major processes, than phasic vestibular neurons, despite the considerably higher firing rates of the former subtype. However, since both neuronal subtypes are indispensable for the encoding and processing of the entire head/body motion dynamics, the higher energy demand of phasic neurons represents an obvious and necessary price to pay. Although phasic and tonic neurons form the respective core elements of the frequency-tuned vestibular pathways, both cellular components are cross-linked through feedforward and feedback side loops. The prominent influence of inhibitory tonic neurons in shaping the highly transient firing pattern of phasic neurons is cost-intensive and contributes to energy consumption for electrical activity in addition to the already extensive energy costs of signal processing by the very leaky phasic vestibular neurons.

Conclusion: Despite the sparse production of action potentials by phasic vestibular neurons, the computation by this neuronal type dominates the ATP expense for processing head/body movements, which might have contributed to the late evolutionary arrival of this central neuronal element, dedicated to the encoding of highly dynamic motion profiles.