Baseline brain energy supports the state of consciousness

Abstract

An individual, human or animal, is defined to be in a conscious state empirically by the behavioral ability to respond meaningfully to stimuli, whereas the loss of consciousness is defined by unresponsiveness. PET measurements of glucose or oxygen consumption show a widespread approximately 45% reduction in cerebral energy consumption with anesthesia-induced loss of consciousness. Because baseline brain energy consumption has been shown by (13)C magnetic resonance spectroscopy to be almost exclusively dedicated to neuronal signaling, we propose that the high level of brain energy is a necessary property of the conscious state. Two additional neuronal properties of the conscious state change with anesthesia. The delocalized fMRI activity patterns in rat brain during sensory stimulation at a higher energy state (close to the awake) collapse to a contralateral somatosensory response at lower energy state (deep anesthesia). Firing rates of an ensemble of neurons in the rat somatosensory cortex shift from the gamma-band range (20-40 Hz) at higher energy state to <10 Hz at lower energy state. With the conscious state defined by the individual's behavior and maintained by high cerebral energy, measurable properties of that state are the widespread fMRI patterns and high frequency neuronal activity, both of which support the extensive interregional communication characteristic of consciousness. This usage of high brain energies when the person is in the "state" of consciousness differs from most studies, which attend the smaller energy increments observed during the stimulations that form the "contents" of that state.

Fig. 1.

Loss of consciousness with anesthesia, as assessed by behavioral output (A) and cerebral metabolism measured by PET (B). Hot colors indicate higher energy demand. [Fig. 1A reproduced with permission from Katoh T, Bito H, Sato S (2000) Influence of age on hypnotic requirement, bispectral index, and 95% spectral edge frequency associated with sedation induced by sevoflurane. Anesthesiology 92(1):55–61.] [Fig. 1B reprinted by permission from Macmillan Publishers Ltd: Alkire MT (2008) Probing the mind: Anesthesia and neuroimaging. Clin Pharmacol Ther 84:149–152, copyright 2008.]

Fig. 2.

¹³C MRS and PET results of baseline energy. (A) Experimental results of V_cyc and CMR_glc(ox),N. Values of V_cyc and CMR_glc(ox),N for the rat brain reported in studies published between 1998 and 2006. The dark blue squares are from Patel et al. (58), the red circle is from Oz et al. (59), the light blue circle is from Choi et al. (60), the green diamonds are from de Graaf et al. (61), and the gray triangles are from Sibson et al. (29). For details of these papers, see ref. . [Reproduced with permission from Hyder et al. (30) (Copyright 2006).] (B) The ratio of V_cyc/CMR_glc(ox),N in the nonanesthetized resting awake state in rat (extrapolated from A; see ·) and human brain (see ref. for details). Similarity of the V_cyc/CMR_glc(ox),N ratio in rats and humans suggests that the relationship between V_cyc and CMR_glc(ox),N are similar. [Reproduced with permission from Hyder et al. (30) (Copyright 2006).] (C) PET image of CMR_glc of the human brain showing uniform and high energy metabolism in the resting, awake state. From ref. with permission. [Reprinted by permission from Wolters Kluwer Health: Alkire MT (2008) Loss of effective connectivity during general anesthesia. Int Anesthesiol Clin 46(3):55–73.]

Fig. 3.

Averaged fMRI maps (from 2 subjects, 2 single runs, 30-s block design, forepaw stimulation) of anterior coronal slices under halothane showed weak widespread activities beyond contralateral primary (S1) and secondary (S2) somatosensory cortices (A), whereas under α-chloralose demonstrated strong localized activation in contralateral S1 (B). Darker colors represent greater overlap across experiments (i.e., reproducibility). All activation maps were thresholded at the same value (P < 0.02). [Copyright 2007 by The National Academy of Sciences of the USA.]

Fig. 4.

Total activity represented by distribution of firing rates (ν; 10-s bins) in the primary somatosensory ensemble of ≈200 neurons for halothane (A) and α-chloralose states (B). Activity under halothane is dominated by the RSN subgroup, which seems unaffected by stimulation. The SSN subgroup, shifting to higher frequencies on stimulation, is similar in both states but more significant under α-chloralose. [Copyright 2007 by The National Academy of Sciences of the USA.]