High metabolic demand in neural tissues: Information and control theory perspectives on the synergism between rate and stability

Evolutionary process has been selected for inherently unstable systems in higher animals that can react swiftly to changing patterns of threat or opportunity, for example blood pressure, the immune response, and gene expression. However, these require continual strict regulation: uncontrolled blood...

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Veröffentlicht in:Journal of theoretical biology 2016-11, Vol.409, p.86-96
1. Verfasser: Wallace, Rodrick
Format: Artikel
Sprache:eng
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Zusammenfassung:Evolutionary process has been selected for inherently unstable systems in higher animals that can react swiftly to changing patterns of threat or opportunity, for example blood pressure, the immune response, and gene expression. However, these require continual strict regulation: uncontrolled blood pressure is fatal, immune cells can attack ‘self’ tissues, and improper gene expression triggers developmental disorders. Consciousness in particular demands high rates of metabolic free energy to both operate and regulate the fundamental biological machinery: both the ‘stream of consciousness’ and the ‘riverbanks’ that confine it to useful realms are constructed and reconstructed moment-by-moment in response to highly dynamic internal and environmental circumstances. We develop powerful necessary conditions models for such phenomena based on the Data Rate Theorem linking control and information theories in the context of inherent instability. The synergism between conscious action and its regulation underlies the ten-fold higher rate of metabolic energy consumption in human neural tissues and implies a close, culturally modulated relation between sleep disorders and certain psychopathologies. •The paper makes formal use of necessary conditions asymptotic limit theorems from information and control theories, via an information bottleneck argument, to examine how high levels of metabolic free energy are needed to both power and stabilize high rates of neural process.•A simple optimization-under-constraint model accounts for wake/sleep duality in highly regulated, high speed neural process, and suggests links with psychopathology.•Control and information theories are used to explore high metabolic rates in neural process.
ISSN:0022-5193
1095-8541
DOI:10.1016/j.jtbi.2016.08.030