Estimating the energy of dissipative neural systems

. 2024 Dec ; 18 (6) : 3839-3846. [epub] 20240829

Status PubMed-not-MEDLINE Jazyk angličtina Země Nizozemsko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39712109

There is, at present, a lack of consensus regarding precisely what is meant by the term 'energy' across the sub-disciplines of neuroscience. Definitions range from deficits in the rate of glucose metabolism in consciousness research to regional changes in neuronal activity in cognitive neuroscience. In computational neuroscience virtually all models define the energy of neuronal regions as a quantity that is in a continual process of dissipation to its surroundings. This, however, is at odds with the definition of energy used across all sub-disciplines of physics: a quantity that does not change as a dynamical system evolves in time. Here, we bridge this gap between the dissipative models used in computational neuroscience and the energy-conserving models of physics using a mathematical technique first proposed in the context of fluid dynamics. We go on to derive an expression for the energy of the linear time-invariant (LTI) state space equation. We then use resting-state fMRI data obtained from the human connectome project to show that LTI energy is associated with glucose uptake metabolism. Our hope is that this work paves the way for an increased understanding of energy in the brain, from both a theoretical as well as an experimental perspective.

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Chen Y, Zhang J (2021) How energy supports our brain to yield consciousness: Insights from neuroimaging based on the neuroenergetics hypothesis. Front Syst Neurosci 15:648860 PubMed PMC

Cranmer M et al. (2020) Lagrangian neural networks. arXiv preprint arXiv:2003.04630

Dezhina Z et al (2023) Establishing brain states in neuroimaging data. PLoS Comput Biol 19:e1011571 PubMed PMC

Dienel GA (2019) Brain glucose metabolism: integration of energetics with function. Physiol Rev 99:949–1045 PubMed

Fagerholm ED, Foulkes W, Friston KJ, Moran RJ, Leech R (2021) Rendering neuronal state equations compatible with the principle of stationary action. J Math Neurosci 11:1–15 PubMed PMC

Friston K (2010) The free-energy principle: a unified brain theory? Nat Rev Neurosci 11:127–138. 10.1038/nrn2787 PubMed

Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273–1302 PubMed

Galijašević M et al (2021) Brain energy metabolism in two states of mind measured by phosphorous magnetic resonance spectroscopy. Front Hum Neurosci 15:686433 PubMed PMC

Galinsky VL, Frank LR (2021) Collective synchronous spiking in a brain network of coupled nonlinear oscillators. Phys Rev Lett 126:158102 PubMed PMC

Gaurav R, Stewart TC, Yi Y (2023) Reservoir based spiking models for univariate time series classification. Front Comput Neurosci 17:1148284 PubMed PMC

Glasser MF et al (2016) A multi-modal parcellation of human cerebral cortex. Nature 536:171–178 PubMed PMC

Gori M, Maggini M, Rossi A (2016) Neural network training as a dissipative process. Neural Netw 81:72–80 PubMed

Gray C, Karl G, Novikov V (1996) Direct use of variational principles as an approximation technique in classical mechanics. Am J Phys 64:1177–1184

Griffanti L et al (2014) ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging. Neuroimage 95:232–247 PubMed PMC

Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500 PubMed PMC

Izhikevich EM (2003) Simple model of spiking neurons. IEEE Trans Neural Netw 14:1569–1572 PubMed

Kirch C, Gollo LL (2021) Single-neuron dynamical effects of dendritic pruning implicated in aging and neurodegeneration: towards a measure of neuronal reserve. Sci Rep 11:1309 PubMed PMC

Magistretti , P. & Allaman, I. in Neuroscience in the 21st century: from basic to clinical 2197–2227 (Springer, 2022).

Margulies DS et al (2016) Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc Natl Acad Sci 113:12574–12579 PubMed PMC

Markello RD et al (2022) Neuromaps: structural and functional interpretation of brain maps. Nat Methods 19:1472–1479 PubMed PMC

Markello RD, Misic B (2021) Comparing spatial null models for brain maps. Neuroimage 236:118052 PubMed

Morse PM, Feshbach H (1954) Methods of theoretical physics. Am J Phys 22:298

Raichle ME (2006) The brain’s dark energy. Science 314:1249–1250 PubMed

Rass V, Helbok R (2019) Early brain injury after poor-grade subarachnoid hemorrhage. Curr Neurol Neurosci Rep 19:1–9 PubMed PMC

Riehl JR, Palanca BJ, Ching S (2017) High-energy brain dynamics during anesthesia-induced unconsciousness. Netw Neurosci 1:431–445 PubMed PMC

Roebroeck A, Formisano E, Goebel R (2011) The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution. Neuroimage 58:296–302. 10.1016/j.neuroimage.2009.09.036 PubMed

Schaefer A et al (2018) Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cereb Cortex 28:3095–3114 PubMed PMC

Shafiei G, Baillet S, Misic B (2022) Human electromagnetic and haemodynamic networks systematically converge in unimodal cortex and diverge in transmodal cortex. PLoS Biol 20:e3001735 PubMed PMC

Shokri-Kojori E et al (2019) Correspondence between cerebral glucose metabolism and BOLD reveals relative power and cost in human brain. Nat Commun 10:690 PubMed PMC

Sosanya A, Greydanus S (2022) Dissipative hamiltonian neural networks: Learning dissipative and conservative dynamics separately. arXiv preprint arXiv:2201.10085

Van Essen DC et al (2013) The WU-Minn human connectome project: an overview. Neuroimage 80:62–79 PubMed PMC

Vaishnavi SN et al (2010) Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci 107:17757–17762 PubMed PMC

Wang R, Wang Y, Xu X, Li Y, Pan X (2023) Brain works principle followed by neural information processing: a review of novel brain theory. Artif Intell Rev 56:285–350

Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12:1–000. 10.1016/S0006-3495(72)86068-5 PubMed PMC

Zhang D, Raichle ME (2010) Disease and the brain’s dark energy. Nat Rev Neurol 6:15–28 PubMed

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