A Functional Account of Stimulation-based Aerobic Glycolysis and its Role in Interpreting BOLD Signal Intensity Increases in Neuroimaging Experiments.

Aug 28, 2023

Experts: Jordan E Theriault,Clare Shaffer,Gerald A Dienel,Christin Y Sander,Jacob M Hooker,Bradford C Dickerson,Lisa Feldman Barrett,Karen S Quigley

In aerobic glycolysis, oxygen is abundant, and yet cells metabolize glucose without using it, decreasing their ATP per glucose yield by 15-fold. During task-based stimulation, aerobic glycolysis occurs in localized brain regions, presenting a puzzle: why produce ATP inefficiently when, all else being equal, evolution should favor the efficient use of metabolic resources? The answer is that all else is not equal. We propose that a tradeoff exists between efficient ATP production and the efficiency with which ATP is spent to transmit information. Aerobic glycolysis, despite yielding little ATP per glucose, may support neuronal signaling in thin (< 0.5µm), information-efficient axons. We call this the efficiency tradeoff hypothesis. This tradeoff has potential implications for interpretations of task-related BOLD "activation" observed in fMRI. We hypothesize that BOLD "activation" may index local increases in aerobic glycolysis, which support signaling in thin axons carrying "bottom-up" information, or "prediction error"-i.e., the BIAPEM (BOLD increases approximate prediction error metabolism) hypothesis. Finally, we explore implications of our hypotheses for human brain evolution, social behavior, and mental disorders.
Copyright © 2023 Elsevier Ltd. All rights reserved.

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ABOUT THE EXPERTS

Jordan E Theriault,Clare Shaffer,Gerald A Dienel,Christin Y Sander,Jacob M Hooker,Bradford C Dickerson,Lisa Feldman Barrett,Karen S Quigley

Jordan E Theriault

Northeastern University, Department of Psychology, Boston, MA. Electronic address: jordan_theriault@northeastern.edu.

Clare Shaffer

Northeastern University, Department of Psychology, Boston, MA.

Gerald A Dienel

Department of Neurology, University of Arkansas for Medical Sciences, Little Rock, AR; Department of Cell Biology and Physiology, University of New Mexico, Albuquerque, NM.

Christin Y Sander

Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA; Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA.

Jacob M Hooker

Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA; Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA.

Bradford C Dickerson

Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA; Department of Neurology, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA; Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA.

Lisa Feldman Barrett

Northeastern University, Department of Psychology, Boston, MA; Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Charlestown, MA; Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA.

Karen S Quigley

Northeastern University, Department of Psychology, Boston, MA; VA Bedford Healthcare System, Bedford, MA.