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Energy consumption and signalling in the white and grey matter of the CNS

Harris, JJ; (2013) Energy consumption and signalling in the white and grey matter of the CNS. Doctoral thesis , UCL (University College London).

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Abstract

Neural computation is energetically expensive, and the brain’s limited energy supply imposes constraints on its information processing capability. How the brain has evolved to perform computational tasks within these energetic constraints is largely unknown. The theoretical and experimental work in this thesis examines how the white and grey matter – which have different computational roles – balance the trade-off between energy consumption and signalling. In the white matter, I show that the maintenance of cellular resting potentials accounts for the largest portion of signalling-related energy use. Maintaining this cost in myelinating oligodendrocytes outweighs the energetic saving on action potentials that myelin provides, but allows for faster action potential propagation. This design places computational benefit above energetic economy. Nevertheless, I show that action potential propagation in the white matter need not rely on metabolic collaboration of axons with oligodendrocytes, and that myelin itself is unlikely to produce ATP as has been proposed. In the grey matter, where synapses account for the largest portion of signalling-related energy consumption, I used electrophysiology to investigate the relationship between information transmission and energy consumption at the retinogeniculate synapse. I found that the number of postsynaptic receptors is set, not to maximise information transmission across the synapse, but to maximise the ratio of information transmitted to energy used on reversing the postsynaptic ion influx. This design places energetic efficiency above computational advantage, as the synapse could theoretically transmit more information if the postsynaptic response were larger. The results of this work suggest that energy supply and demand have played critical roles in shaping the way that the brain has evolved to process information, both in the white and grey matter. We should keep these energetic factors in mind when considering the brain’s adaptation to any computational task. The thesis also contains a description of experiments investigating mitochondrial trafficking in oligodendrocytes, and searching for plasticity of conduction speed in the white matter. A review of how energy supply to the brain alters with age, and how this may affect the BOLD (blood oxygenation level dependent) signal, is included as an Appendix.

Type: Thesis (Doctoral)
Title: Energy consumption and signalling in the white and grey matter of the CNS
Language: English
Additional information: Permission for digitisation not received.
UCL classification: UCL > Provost and Vice Provost Offices
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Neuro, Physiology and Pharmacology
URI: https://discovery.ucl.ac.uk/id/eprint/1399237
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