Toward a Science of Consciousness, Day 2: Baseline Brain Energy Supports the State of Consciousness

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One of the other presentations this morning focused on the brain's use of energy as a substrate for consciousness. Robert G. Shulman teaches at Yale, so I should probably take this more seriously than I do - but it seems like common sense when you boil it down to its basic facts.

Baseline Brain Energy Supports the State of Consciousness. Robert G. Shulman (Molecular Biophysics & Biochem, Yale University, New Haven, CT)

^ 13 C MRS measurements of the Cerebral Metabolic Rate of Glucose Oxidation and of the coupled Glutamate Neurotransmitter flux (1) showed that >80% of brain energy in the rat or human is devoted to supporting the work of neuronal firing in contrast to earlier proposals of an inefficient use of energy. Calibrations of the fMRI BOLD signals showed that their energy consumption was of the order of a few percent of the total energy.(2) These values refuted the model of a computer-like brain which only did work when stimulated and showed that positive and negative BOLD signals were both small differences of large firing activities.(3) Subsequently multi-unit electrical recordings of the rat brain(4) showed that during sensory stimulation a large fraction of the neurons in the somato-sensory cortex changed their firing rates with a majority firing faster and a minority slower. The high level of global energy (and firing) has been studied by ^ 13 C MRS during anesthesia in the rat with results that resemble the several PET studies of humans(5). The person,or the rat, in a State of Consciousness, as determined by its observable response to stimuli, looses awareness with deepening anesthesia until the global energy is decreased by ~50% beyond which it is no longer aware of stimuli. FMRI BOLD patterns change significantly with deepening anesthesia and histograms of neuronal firing show the loss of high frequencies in the ~40Hz. range.High global energy serves the supporting role that Christof Koch had postulated as the enabling Neuronal Correlates of Consciousness,(NCCe), needed to bring focal responses to sensory stimulation to a higher awareness. Physical understanding of neuronal energy and work have allowed us to reliably determine brain properties of the person in the State of Consciousness, identified from observable behavior, and have eliminated the need to postulate imprecise psychological processes.
(1) Sibson,N et al Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):316-21
(2) Hyder F,et al.(2001) NMR Biomed 14:413-431.
(3) Shulman,R.G. & Rothman,D.L.Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10765-70.
(4) Smith. A. et al (2002) Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10765-70.
(5)Alkire MT, Hudetz AG &Tononi G (2008) Consciousness and anesthesia. Science 322:876-880.
(6) Shulman, R.G. et al Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11096-101.

This was an interesting talk, but once he got past explaining the glutamate/glutamine energy system in the brain, the main point was that a fully conscious brain (100%) uses more energy that a deep-sleeping brain or comatose brain or a vegetative brain (40-60%), and a dead brain (0%).

Midline structures in the brainstem and thalamus necessary
to regulate the level of brain arousal.

Christof Koch has suggested that in order for there to be Neural Correlates of Consciousness (NCC), there has to be an eNCC, an enabling NCC. Shulman suggests that the eNCC is "global high baseline energy."

You can read his whole article here, courtesy of PNAS. What follows is the introduction, which offers a bit more info than the abstract:

The excitement in modern neuroscience anticipates relating brain activity to mental processes of behavioral states, such as consciousness. In recent years, fMRI, ¹³C magnetic resonance spectroscopy (MRS), PET, and electrophysiology experiments have been directed toward these goals. These studies have measured brain energy production in the form of glucose oxidation in the resting awake state and the anesthetized state, and have followed regional changes during stimulation from these states. The most striking result is that the total energy consumption supporting neuronal firing in the conscious awake, baseline state is orders of magnitude larger than the energy changes during stimulation (1–3). Nonetheless, most research relating brain activity to mental processes has been based on the smaller fMRI or PET increments, which generally are interpreted as localizing psychological concepts. Early functional imaging studies by Posner and Raichle (4), using PET scans, posited that a connection between mental concepts and brain activities can be made by the difference in the images obtained when the assumed mental concept, or module, was or was not involved in a task (e.g., by comparing brain images of a subject reading proper and nonsense words). Differences between 2 functional images were interpreted as providing a quantitative map that localized the neuronal underpinnings of the mental modules; in the case at hand, that mental activity would be semantics. This experimental paradigm was soon adopted for fMRI studies, a technology which made functional brain imaging widely accessible.

However, it soon became clear that the brain response to cognitive subtraction did not follow the simplistic assumptions of “pure insertion,” but rather depended on the context of the task. The dependence of brain responses on their context created problems for cognitive psychology. Jerry Fodor, a founder of the field, concluded in 2000 that the mind does not work that way (5), because the dependence on context undercut the causality claimed for the concepts of cognitive neuroscience. Results, including the influence of context in psychologically-based fMRI or PET studies, led us, in 1996, to question the value of such concepts for functional brain imaging. We suggested that the field would be better served by using the functional imaging data to question cognitive concepts, rather than by considering those assumptions proven when a difference image is acquired (6).

However, prominent neuroimagers retained the potential value of the cognitive concepts, and considered that the loss of pure insertion might arise from the nonlinear nature of brain responses (7). Parametric methods were designed to overcome brain nonlinearity and to more closely relate brain responses to the input activities (8). However, in these studies, the search for brain responses to psychological concepts remained the goal. A strong version of that goal, that represents the popular position of pure insertion despite empirical set-backs, was described by Gazzaniga (9), who says that “we now understand that changes in our brain are both necessary and sufficient for changes in our mind,” and continues by praising cognitive neuroscience for studying the mechanisms of cognitive phenomena.

This report studies the support of behavior by brain activity without making mentalistic/psychological assumptions about the unobserved processes presumably involved in observed behaviors or behavioral states and finds a necessary role for the unassigned high baseline energy. In both of these respects, it offers a previously untried methodology for relating brain activities to mental processes. We believe that brain activities provide necessary support for behavioral processes that are performed and experienced by the human (or rodent) in the state of consciousness. In our study, brain experiments are used to determine neuronal and energetic properties of a behavioral state, as distinguished from the claims that imaging results localize in the brain the mental processes that cause a cognitive conceptualization of behavior. Brain activities support and are properties of a person in a behavioral state, such as consciousness, and they, thus, enable mental processes such as remembering or intending, all of which contribute to being conscious. Instead of aiming to localize assumptions about the nature of a mental process, we start with a behavioral index that the individual is in the conscious state and then measure neuronal properties of that state. Rather than localizing psychological assumptions which, in Zeman's description (10), would form the contents of consciousness, the subjects (rat or human) are defined as being in a conscious state by observations of reproducible behavior.

The state of consciousness is defined by the subject's ability to respond to stimuli using the criteria established in anesthesia (11). The object of study should be the person, an entity which includes brain, body, and mental processes, that cooperate to interact with the environment. This position has been championed by Antonio Damasio who, as a neurologist and neuroscientist, has written compelling books in support of the idea that the study of “mental activity, from its simplest aspects to its most sublime, requires both brain and body” (12). The neurophysiological basis of his belief is documented in an account of how body and brain are in continual back and forth interactions via chemical and neuronal impulses. Our position also resonates with a comprehensive analysis of cognitive neuroscience developed by Bennett and Hacker (13). Their criticism is that mental functions are performed by the person; therefore, they are not located, represented, or encrypted in a brain. A person adds, subtracts, feels pain or decides to marry, not the brain. In this interpretation, brain activities can be necessary for a person's behavior, but they are not sufficient to explain it.

We propose that high baseline energy (therefore, the neuronal activity) in the awake state is a necessary property of the conscious state; when the energy is reduced sufficiently, there is loss of consciousness. Two additional brain properties measured are the significant changes in fMRI activation patterns and the neuronal population activity at different baseline energy states. Implications for philosophies and theories of the conscious state are discussed to demonstrate how measurable brain properties can allow a physical understanding of the state without psychological assumptions. The role of consciousness in the different stages/types of sleep or seizure (14) are beyond the scope of the current report.

Hmmmm . . . .

My response was, "So what?"

Yes, consciousness in the brain requires energy metabolism. Therefore, high baseline global energy is necessary, but not sufficient for consciousness. It doesn't take 40 minutes to say that, only to demonstrate one particular mechanism of how that happens, the glutamatergic neurotransmission model.

The basic underlying assumption, which was not stated, is the consciousness requires a brain - and I do not really argue with this assumption.

Tags: brain, consciousness, energy, glutamatergic neurotransmission, neuroscience, Toward a Science of Consciousness, Day 2, Baseline Brain Energy Supports the State of Consciousness, Robert G. Shulman, brain states, energy consumption, waking, deep sleep, vegetative states, coma, anesthesia, brain death