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Modeling of Pathophysiological Coupling between Brain Electrical Activation, Energy Metabolism and Hemodynamics: Insights for the Interpretation of Intracerebral Tumor Imaging

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Abstract

Gliomas can display marked changes in the concentrations of energy metabolism molecules such as creatine (Cr), phosphocreatine (PCr) and lactate, as measured using magnetic resonance spectroscopy (MRS). Moreover, the BOLD (blood oxygen level dependent) contrast enhancement in functional magnetic resonance imaging (fMRI) can be reduced or missing within or near gliomas, while neural activity is not significantly reduced (so-called neurovascular decoupling), so that the location of functionally eloquent areas using fMRI can be erroneous. In this paper, we adapt a previously developed model of the coupling between neural activation, energy metabolism and hemodynamics, by including the venous dilatation “Balloon model” of Buxton and Frank. We show that decreasing the cerebral blood flow (CBF) baseline value, or the CBF increase fraction, results in a decrease of the BOLD signal and an increase of the lactate peak during a sustained activation. Baseline lactate and PCr levels are not significantly affected by CBF baseline reduction, but are altered even by a moderate decrease of mitochondrial respiration. Decreasing the total Cr and PCr concentration reduces the BOLD signal after the initial overshoot. In conclusion, we suggest that the coupled use of BOLD fMRI and MRS could contribute to a better understanding of the neurovascular and metabolic decoupling in gliomas.

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Authors and Affiliations

  1. INSERM U 483, Université Pierre et Marie Curie, Boîte 23, 9 quai Saint-Bernard, 75252, Paris Cedex 05, France

    Agnès Aubert & Robert Costalat

  2. INSERM U 494, CHU Pitié-Salpêtrière, 91 Boulevard de l'Hôpital, 75634, Paris Cedex 13, France. E-mail

    Agnès Aubert, Hugues Duffau & Habib Benali

  3. Department of Neurosurgery, 47-83, Boulevard de l'Hôpital, 75651, Paris Cedex 13, France

    Hugues Duffau

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  1. Agnès Aubert
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  2. Robert Costalat
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  3. Hugues Duffau
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  4. Habib Benali
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Aubert, A., Costalat, R., Duffau, H. et al. Modeling of Pathophysiological Coupling between Brain Electrical Activation, Energy Metabolism and Hemodynamics: Insights for the Interpretation of Intracerebral Tumor Imaging. Acta Biotheor 50, 281–295 (2002). https://doi.org/10.1023/A:1022620818701

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