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New Approaches to Functional Neuroenergetics Meeting Report New Approaches to Functional Neuroenergetics Susan M. Fitzpatrick Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/11/4/467/1758540/089892999563454.pdf by guest on 18 May 2021 James S. McDonnell Foundation Douglas Rothman Yale University glucose metabolism. Depending on the form of the la- INTRODUCTION beled tracer used, PET either directly measures the re- gional rate of glucose metabolism (CMRglc) or the The coupling between brain energy metabolism and coupled parameters of the cerebral metabolic rate for neuronal activity has, for more than a century, allowed oxygen (CMRO2), and the cerebral blood ºow (CBF) rate. researchers to monitor brain function (Roy & Sher- The fMRI blood oxygenation level dependent (BOLD) rington, 1890; Siesjo, 1973; Sokoloff, 1981). A break- signal is sensitive to both CMRO2 and CBF (Ogawa et al., through in this effort, and one that made human studies 1998). routine, was the development 20 years ago of positron In a functional imaging study, a subject performs ex- emission tomography, or PET (see Raichle, 1998). In perimental tasks while the signal is acquired. Most cog- combination with experimental paradigms and models nitive neuroscience imaging studies rely on the PET CBF developed in cognitive psychology, PET allowed the ªrst or the BOLD fMRI measurement. The acquired signal is high-resolution metabolic maps of functionally special- analyzed to provide images of the spatial distribution and ized regions of the human brain. A drawback of the PET temporal dynamics of CBF or BOLD contrast. The func- technology was its reliance on cyclotron-generated tional image is an image of the increment in signal short-lived radioisotopes. The subsequent development intensity during a task relative to a baseline state in of functional magnetic resonance imaging (fMRI) made which the subject rests in the scanner. Cognitive proc- functional brain mapping widely available to scientists esses are localized by functional imaging using experi- (Kwong et al., 1992; Ogawa, Menon, Kim, & Ugurbil, mental paradigms and analyses based upon theories of 1992). Almost weekly, new brain imaging results are cognitive neuroscience. highlighted in scientiªc journals and the popular media As an illustrative example, consider a study designed as providing new insights into the biological basis of to assess whether the frontal lobe is involved in the human brain function and neurological and psychiatric general cognitive skill of verbal working memory. The disorders. subject would perform tasks requiring this cognitive The application of PET and fMRI to localize cognitive skill, such as remembering lists of words, while being processes is based on the assumption that functional scanned. In one strategy the degree of involvement of neuronal activity increases when a region is involved in verbal working memory in each task would be varied, performing a cognitive task (Posner & Raichle, 1994). but the requirements for other cognitive skills would be These functional neuronal activities are involved in the held constant. The relative intensity of the functional communication of information between neurons and imaging signal in the frontal lobe during each task would include neurotransmitter release and action potentials. be statistically correlated with the verbal working mem- The energy required for these and other brain processes ory component. A positive correlation would support is provided almost exclusively by oxidative glucose me- the involvement of frontal lobe neuronal activity in this tabolism (Siesjo, 1978). Functional imaging measures skill (Posner & Raichle, 1994, provides an excellent sum- either glucose metabolism or neurophysiological pa- mary of how imaging studies are designed). rameters coupled to glucose metabolism (Sokoloff, Given the enthusiasm with which functional imaging 1981). Regions of increased functional neuroenergetic is used to answer sophisticated questions about the demand are identiªed by the corresponding increase in functional architecture of the brain, it is easy to forget © 1999 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 11:4, pp. 467–471 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892999563454 by guest on 29 September 2021 that there are long-standing controversies concerning of metabolism with development) deªnitive answers the neuroenergetic basis of the signal. To deªne some of would be obtained for these fundamental, long-standing the outstanding questions that remain in the ªeld, and questions. to encourage research to better understand the meaning of these measurements, the James S. McDonnell Founda- What are the molecular mechanisms that couple tion organized a workshop, Cerebral Metabolism and neuroenergetic requirements to CMRglc and CMRO2? Human Cognition: A Workshop Discussing New Ap- Although most functional neuroimaging studies assume proaches to Functional Neuroenergetics.1 The workshop that signal changes reºect neuronal activity, Pierre Magi- took place over two days with focused talks and ani- stretti (University of Lausanne) presented results identi- mated discussions on a variety of issues related to fying the astrocyte as the primary site of cerebral Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/11/4/467/1758540/089892999563454.pdf by guest on 18 May 2021 neuroenergetics and functional imaging. Some of the glucose consumption. Magistretti proposed that astro- major questions identiªed and the results of these dis- cytic glucose uptake is mechanistically coupled to cussions are described in this report. Selected references neuronal energy requirements by the use of nonoxida- are provided for key points raised by the participants. tive glycolysis to provide energy for removing glutamate, released by the nerve terminals, from the synaptic cleft. What is the relationship between the imaging signal The lactate produced as a result of the incomplete oxi- being acquired and the cellular localization of neuro- dation of glucose is then transported from the astrocyte nal activity? to the neuron as a substrate for oxidative energy meta- Louis Sokoloff (NIMH) reviewed studies on the cellular bolism (Pellerin et al., 1996). Robert Shulman’s in vivo location of glucose metabolism in peripheral neurons. results from rat and human brain supported and ex- These studies showed that the uptake of radio-labeled tended the proposal by Magistretti. Shulman described deoxyglucose during electrical stimulation of peripheral 13C NMR spectroscopic studies showing that the rate of neurons occurs mainly in the synaptic regions. The rate astrocytic glutamate uptake increased with glucose me- of glucose metabolism was close to linear with the tabolism with close to a 1:1 stoichiometry (Sibson et al., stimulation frequency, which he interpreted as support- 1998). He proposed that 80% of cortical glucose oxida- ing a direct relationship between increases in CMRglc tion is coupled to neuronal glutamate release and uptake measured by PET and the total electrical activity of a by the astrocyte. Rolf Gruetter (University of Minnesota) region (Yarowsky, Kadekaro, & Sooloff, 1983). Gordon discussed his own 13C NMR spectroscopy data of human Shephard (Yale University) addressed the issue of the brain with enhanced sensitivity that is consistent with variations in neuroenergetic requirements as a function Shulman’s ªndings (Gruetter, Seaquist, Kim, & Ugurbil, of cell type and brain region. He pointed out that the 1998). A lively discussion initiated by Albert Gjedde (Uni- relationships measured in peripheral neurons do not versity of Denmark) questioned the localization of glu- hold for all classes of neurons. He presented high-reso- cose metabolism to the astrocyte. Among the objections lution deoxyglucose autoradiography studies of the ol- were the presence of a high glucose transporter and factory bulb that showed that unmyelinated axons have glycolytic enzyme capacity in neurons as well as the lack a high glucose metabolic rate (Greer, Stewart, Kauer, & of direct evidence in vivo. Although no consensus was Shepherd, 1981). Because unmyelinated axons are com- reached, it was agreed that the results presented pro- mon in the cerebral cortex, they may contribute sig- vided important new insights into the potential coupling niªcantly to the neuroenergetic requirements measured of the functional imaging signal to neurotransmission. by functional imaging. Shepherd, collaborating with Yale colleague Robert Shulman, is correlating metabolic and Are functional neuroenergetic requirements tempo- electrical maps of neuronal activity in the olfactory bulb rally dependent? with ultra-high-resolution fMRI (Yang et al., 1998). Wil- Marcus Raichle (Washington University) and Louis Sok- liam Greenough (University of Illinois) observed that oloff each presented data suggesting, in the human and functional imaging of the developing or learning brain, rat brain, respectively, that the fractional increase in in which the density of synapses and other neuronal CMRglc is greater than CMRO2 during sensory stimula- structures changes with time, may help in the assign- tion. Mark Mintun (Washington University) discussed his ment of the neuroenergetics measured by functional recent PET results, showing that at longer stimulation imaging to speciªc cellular structures. Along these lines times CMRO2 increases, consistent with NMR and mi- Kevin Behar (Yale University) discussed NMR measure- crodialysis data showing a transient increase
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