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Sympathetic Innervation of the Pupil Is Affected Is Good to See As Many Of > Book Reviews 2365 sympathetic innervation of the pupil is affected is good to see speci®c mechanisms coupling metabolic and physiological as many of my students fail to be convinced of its existence changes to changes in neuronal activity. for the reason that it is not possible to demonstrate to them the This slim volume leads the reader at an almost descending pathways in Weigert-stained brainstem sections. breathless pace from classical studies through to the Part 8 is entitled `Functional Neuroanatomy and Patho- most recent work concerning activity-coupled brain physiology: Clinical Correlations' and that's exactly what it energy metabolism. As a report of a workshop held contains. Once again a melange of CT scans, MRIs, between a small group of research leaders in different photographs, pathological sections of autopsy material prin- areas with expertise converging on common problems, it cipally focusing on cerebrovascular lesions provide excellent manages to be more current than recent textbooks. It is reference material. Other examples of neuropathology are also comprehensive, despite its brevity. It gives the reader Downloaded from https://academic.oup.com/brain/article/125/10/2365/300399 by guest on 30 September 2021 also included such as Alzheimer's disease, striatonigral a very clear sense of the way in which our understanding degeneration and gliomas. Also, there are interesting is changing and identi®es areas of continued uncertainty. examples of neurobehavioural changes associated with The editors and co-editors have done an excellent job in neurological conditions included in this part. establishing a coherent style and in maintaining a All in all a wonderful atlas of neuroanatomy of great value consistent set of themes through the book. to any student, of whatever level, of neuroanatomy and of It may be surprising to readers unfamiliar with the area, but course to clinical neurologists as well. But, it does have two fundamental issues of brain energy metabolism still are being aspects which, to my mind, confer an overt impression of a reformulated. It has long been recognized that the brain, only lack of contemporary thinking. First, the rather heavy, representing 2% of the body weight, consumes an inordin- highlighted leader lines on many of the ®gures could have ately high 20% of the body's energy. Yet the way in which been replaced by a more subtle system of lettering or this energy is used has been (curiously) uncertain. Classical numbering as well as the black borders to the pages of studies by Creuzfeldt based on thermal measurements of the illustrations. Secondly, the lack of CT and MRI images peripheral nerve lead to the widely accepted (but somewhat interspersed among the sectional images, similarly numbered counter-intuitive) conclusion that the direct consequences of for comparison, would have elevated the atlas into the realms neuronal depolarization account for only a small proportion of the perfect companion for the study of neuroanatomy for of energy consumption in the brain. If true, this conclusion students and clinicians alike. certainly should raise questions about the interpretation of localization of neuronal activity (at least as related to Robert M. Santer electrophysiological studies) based on physiological or School of Biosciences 2, biochemical changes. Cardiff University, Frackowiak and Maguire open the book with a short and Cardiff, UK selective review of evidence that metabolic mapping can well localize neuronal activity, providing illustrative examples in which PET and fMRI studies show a close correspondence with evidence from both human psychophysical and animal NEUROENERGETICS: RELEVANCE IN FUNCTIONAL studies. This theme is taken further in a report of very high BRAIN IMAGING magnetic ®eld studies by Kamil Ugurbil and Seigi Ogawa By R. S. J. Frackowiak, P. J. Magistretti, R. G. Shulman, who focus speci®cally on the blood oxygenation level- J. S. Altman and M. Adams dependent (BOLD) fMRI signal. The very high ®eld strengths 2002. Strasbourg: Human Frontier Science Program allow both increased sensitivity and spatial localization and Organization Ugurbil and Ogawa demonstrate that localization of acti- ISBN 9291640107 vation-related BOLD signal changes is not only entirely consistent with electrophysiological measurements, but also Perhaps the major goal for cognitive neuroscience is to de®ne that the time course of changes is just as predicted by direct the ways in which the activity of aggregates of neurones observation of local haemoglobin oxygenation changes by create phenomena of mind. Brain functional imaging is optical imaging studies. proving to be one of the most versatile tools for working The brain is a highly oxidative organ. Neurones have a high towards this goal. Two of the most powerful approaches have oxidative capacity and the brain has only a limited capacity been positron emission tomography (PET) and, more for anaerobic metabolism. However, PET studies from recently, functional magnetic resonance imaging (fMRI). Marcus Raichle's laboratory in St Louis in the mid-1980s However, both provide only indirect measures of neuronal provided a challenge to this notion that has yet to be fully activity. Instead, they measure local changes in brain resolved. In careful experiments measuring the local changes metabolism and physiology that are associated with neuronal in cerebral blood ¯ow, cerebral oxygen and glucose con- activity. As interest has developed in applying these methods sumption, Raichle and his colleagues noted a curious quantitatively, it has become critically important to under- discrepancy. While blood ¯ow increases are large in regions stand the nature of the signals being measured and thus, the local to neuronal activation and are associated with propor- 2366 Book Reviews tional increases in glucose consumption, increases in oxygen extra-neuronal space. Returning from the biochemistry to the consumption are much more limited, suggesting a local local cytoarchitecture, Fillenz reminds the reader of the close `uncoupling' of oxygen and glucose utilization. This obser- juxtaposition of the foot processes of astrocytes on capillar- vation suggests that the brain metabolises glucose anaerobi- ies. Glucose transporters are found on these processes and cally (at least to an extent) during the activation response. tight junctions should limit any passive ¯ow of glucose from Different contributors to the book approach this central the capillary into the extra-cellular space elsewhere. This problem in distinct ways. Pierre Magistretti and Luc Pellerin structural organization suggests that the astrocyte might have set out a very speci®c hypothesis regarding the nature of provide the key conduit for glucose from the blood to the the uncoupling which has driven the ®eld forward substan- neurone. Local glucose concentrations then could be coupled tially by providing clearly testable ideas. Starting from the via sensitivity to glutamate release to increased metabolic Downloaded from https://academic.oup.com/brain/article/125/10/2365/300399 by guest on 30 September 2021 observation that astrocytes have relatively high concentra- needs for synaptic activity. tions of glycolytic enzymes and glycogen, while mitochon- Such a mechanism puts the question of substrate provision dria are more abundant in neurones, Magistretti and his central to understanding brain activity. Not only could the colleagues argue that there may be a specialized form of astrocytes act to facilitate glucose transport, they also may act metabolic coupling between the two different cell types. as local stores of glucose equivalents that can be mobilised Astrocyte processes are found in close relationship to the for rapid increases in energy consumption with neuronal synapse. According to the Magistrettti±Pellerin hypothesis, activation. This could be determined by local neurotransmit- glucose uptake in the relatively glycolytic astrocytes may be ter release. Astrocytic glycogenolysis (hydrolysing glycogen preferentially used for lactate production, which, when to glucose) is stimulated by increases in cAMP, which can be released, can then be utilized by nearby neurones to fuel driven, for example, by neuroadrenergic stimulation or oxidative metabolism. Given that glutamate transport into release of vasoactive intestinal peptide (VIP). Neuro- astrocytes is linked to increased glucose utilization and adrenergic stimulation is a known diffuse modulator of lactate production, the glutamate release from excitatory neuronal function. VIP release occurs via more speci®c synapses could directly coordinate this local metabolic cycle mechanisms, consistent with functions as a local modulator of by linking to glucose utilization in astrocytes. neuronal activity. Both neurotransmitters potentially could The elegant animal studies of Doug Rothman, Bob `facilitate' neuronal activity by the common metabolic effects Shulman and their colleagues at Yale is presented to of promoting glycogenolysis from astrocytes. Given that each complement this work in vitro. The Yale group has pioneered astrocyte contacts 30 000±40 000 synapses (about the number applications of magnetic resonance spectroscopy to func- on approximately eight pyramidal neurones) such a mechan- tional imaging and demonstrated the predicted coupling ism would provide an additional way of coordinating activity between glutamate±glutamine cycling and glucose utiliza- in larger neuronal aggregates. tion. With a two-compartment model such as that
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