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The dark matter of the brain

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Abstract

The bulk of brain energy expenditure is allocated for maintenance of perpetual intrinsic activity of neurons and neural circuits. Long-term electrophysiological and neuroimaging studies in anesthetized and behaving animals show, however, that the great majority of nerve cells in the intact brain do not fire action potentials, i.e., are permanently silent. Herein, I review emerging data suggesting massive redundancy of nerve cells in mammalian nervous system, maintained in inhibited state at high energetic costs. Acquired in the course of evolution, these collections of dormant neurons and circuits evade routine functional undertakings, and hence, keep out of the reach of natural selection. Under penetrating stress and disease, however, they occasionally switch in active state and drive a variety of neuro-psychiatric symptoms and behavioral abnormalities. The increasing evidence for widespread occurrence of silent neurons warrants careful revision of functional models of the brain and entails unforeseen reserves for rehabilitation and plasticity.

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Fig. 1

d, f Adapted with permission from (Andersen et al. 1964)

Fig. 2

Adapted with permission from Corkin et al. (1997) and Forsdyke (2014) and MRI brain atlas (http://w-radiology.com/atlas_brain_mri.php)

Fig. 3

Adapted with permission from Spencer et al. (2008)

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Acknowledgements

This review is dedicated to the memory of Dr. Oliver Sacks. The author would like to thank Drs. R. Llinas, G. Buzsaki, M. Raichle, N. Logothetis and other leaders in the field of neuroscience and neuroimaging for their excellent research and inspiring articles and books. Special thanks go to Dr. V. O’Leary for insightful discussions and for proofreading the manuscript. The author would like to thank the National Sustainability Program 1 of the Czech Republic for supporting ongoing research projects (nr. LO1611) within the Department of Experimental Neurobiology at the National Institute of Mental Health, Czech Republic.

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Ovsepian, S.V. The dark matter of the brain. Brain Struct Funct 224, 973–983 (2019). https://doi.org/10.1007/s00429-019-01835-7

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