Updated Energy Budgets for Neural Computation in the Neocortex and Cerebellum

Abstract

The brain's energy supply determines its information processing power, and generates functional imaging signals. The energy use on the different subcellular processes underlying neural information processing has been estimated previously for the grey matter of the cerebral and cerebellar cortex. However, these estimates need reevaluating following recent work demonstrating that action potentials in mammalian neurons are much more energy efficient than was previously thought. Using this new knowledge, this paper provides revised estimates for the energy expenditure on neural computation in a simple model for the cerebral cortex and a detailed model of the cerebellar cortex. In cerebral cortex, most signaling energy (50%) is used on postsynaptic glutamate receptors, 21% is used on action potentials, 20% on resting potentials, 5% on presynaptic transmitter release, and 4% on transmitter recycling. In the cerebellar cortex, excitatory neurons use 75% and inhibitory neurons 25% of the signaling energy, and most energy is used on information processing by non-principal neurons: Purkinje cells use only 15% of the signaling energy. The majority of cerebellar signaling energy use is on the maintenance of resting potentials (54%) and postsynaptic receptors (22%), while action potentials account for only 17% of the signaling energy use.

Energy Demand of Synaptic Transmission at the Hippocampal Schaffer-Collateral Synapse

“…1,2,6,7,20 In terms of ATP use, calculated expenditure for the cortex were 50% on postsynaptic potentials, 21% on APs, 20% on resting potentials, and 9% on presynaptic processes. 7 When the costs for resting potentials are not taken into account, these values renormalize to 62.5%, 26.25%, and 11.25% for postsynaptic processes, APs, and presynaptic processes, respectively. In our experiments, about 18% of the oxygen used was spent on presynaptic APs and about 30% on presynaptic process other than APs.…”

“…3--5 Recalculating the energy need for APs suggests larger contribution of postsynaptic and presynaptic processes and transmitter uptake to the energy demand of synaptic transmission. 6,7 The authors predicted that in cerebral cortex, 50% of signaling associated energy is spent on restoration of ion fluxes at postsynaptic glutamate receptors, 21% is spent on APs, 20% on resting potentials, 5% and 4% on presynaptic transmitter release and transmitter recycling, respectively. However, such numbers have to be calculated or determined experimentally for each brain area in question as synaptic densities, receptor types, and ion channel expression differ for each particular signaling pathway.…”

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

“…3,76 In primates, the synaptic costs might be even larger because of the higher numbers of synapses per neuron. 76 Other studies also suggested that the major neuronal energy utilization is for excitatory synaptic signaling (neuronal input) rather than action potentials of the axon (neuronal output). 60,[77][78][79] This might be reflected by the strong linear correlation between synaptic activities, oxygen metabolism, and cerebral blood flow in vivo, at least for some experimental stimulation paradigms.…”

“…61,80 In contrast to the excitatory projection cells, estimates about energy costs of inhibitory interneurons are widely lacking because of insufficient experimental data and cell-specific neuroenergetic knowledge. 18,76 Few studies from hippocampus and neocortex provide first evidence that (i) glucose metabolism is increased during long-term recurrent inhibition of hippocampal pyramidal cells, 81 (ii) the contribution of GABA to the glutamate/GABA-glutamine cycle might account for 10% to 15% of the total oxidative metabolism 82 and (iii) glucose metabolism might be significantly stronger in GABAergic neurons than in glutamatergic neurons as revealed by combining high-resolution 2-deoxyglucose and immunohistochemistry. 83 For the latter technically advanced study with single-cell resolution, the methodological obstacles such as adequate label retention during immunohistochemical processing that may limit interpretation have been discussed.…”

The Oxygen Paradox of Neurovascular Coupling

“…1,2 The oxygen-glucose index of the brain is close to six in the resting state, 3,4 thus the brain consumes, on average, six molecules of oxygen per molecule glucose. The high-energy demand generates the need for a large amount of oxygen delivered via the blood stream.…”