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Brain (2008), 131, 2798 ^2801 BOOK REVIE W Cicero’s brain and vibrating nerves Few pairs of books about the history of the brain could be more discordant than this one. Daniel Lord Smail, a Harvard historian, makes a strong plea for integrating the general history of mankind with the evolutionary history of the brain. No mean task, certainly not for someone whose first book, published in 1999, examined changes in spatial designation in the notarial registries of medieval Marseille. The other book, edited by Whitaker, Smith and Finger, contains a collection of essays about 18th century advances in understanding of the nervous system. Despite their disparate vantage points, the pairing serves as a reminder that the organ of neuroscience is not immutable but evolving—however slowly. The first three chapters of Smail’s book are a passionate vindication of ‘deep history’, that is, history beginning at least with the emergence of Homo sapiens sapiens in Africa, some 140 000 years ago. In his eyes, the ‘prehistoric’ era should not be left to geologists, anthropologists and archaeologists. When Palaeolithic tribes migrated to Europe and Asia, some 85 000 to 50 000 years ago, humans were still migrant hunters, with an economy ‘based on the calorie’. Probably it was by sheer necessity—prey having become scarce—that around 10 000 years ago the nomadic way of life gave way to a sedentary, agricultural society: the Neolithicum or late Stone Age. Remarkably, this transition took place at roughly the same time in different continents. Most historians, however, limit their narrative to history since the Bronze Age, 5500 years before our time, when also nation states developed. Smail chides his colleagues for their ‘myopic view’ and ‘sterile presentism’, hardly disturbed by the time revolution of the 1860s articulated in Darwin’s ‘On the origin of species’ (1859), Lyell’s ‘The geological evidences of the antiquity of man’ (1863) and Lubbock’s ‘Pre-historic times’ (1865). The habit of starting history with Mesopotamia (or with Egyptian culture, popular in the 19th century) he regards as a lame substitute for the traditional biblical signposts: the Garden of Eden, the deluge or the destruction of the Tower of Babel. Smail punctiliously and eloquently dissects the resistance of historians against inclusion of the Stone Age in regular history. Their most common argument, of course, is the lack of written records. For that reason the ‘speechless past’ is often regarded as a stagnant buffer zone, before ‘true history’ began. But other disciplines have adopted a broader definition of ON DEEP HISTORY AND THE BRAIN. By Daniel Lord Smail 2008. Berkeley: University of California Press Price: £12.95 ISBN: 978-0-520-25289-9 BRAIN, MIND AND MEDICINE – ESSAYS IN EIGHTEENTH-CENTURY NEUROSCIENCE. Edited by Harry Whitaker, C. U. M. Smith and Stanley Finger. 2007. New York: Springer Price: $36.00 ISBN: 978-0-387-70966-6 ‘documents’: lumps of rock, fossils, mitochondrial DNA, isotopes, behavioural patterns, potsherds, phonemes and cave paintings. Spoken language, not written language, should be the defining characteristic of mankind, one that may well have been present in earlier hominins than H. sapiens sapiens. A more complex argument for the tradition of setting ‘prehistory’ apart is the assumption that history should take account only of the period characterized by ß The Author (2008). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: [email protected] Book Review ‘cultural evolution’, the transmission of rites and knowledge to subsequent generations. Darwinian evolution is biology, not history, as the reasoning has it. Smail disagrees and argues that it is impossible to attach a date to the point of rupture where Darwinian selection would have been replaced by cultural transmission. That he designates cultural evolution as ‘(neo)Lamarckian’ is a little confusing, since intergenerational transmission occurs exclusively by learning and relearning and not by biological transmission of acquired traits, as Lamarck (1744–1829) would have it. In the pivotal fourth chapter, ‘The new neurohistory’, enters the brain centre-stage. Smail starts from two premises. First, cultural factors not only heavily influence behaviour, but may even become ‘hardwired’ into the brain. Second, genetic influences on behaviour should not be simplified as ‘one gene, one behavioural trait’, as in the ‘gene for blue eyes’, but rather as determining a multitude of ‘behavioural modules’, engineered by natural selection. These modules may or may not be expressed, depending on the environment. They may also be used for ends other than those best served at the time the original adaptive trait emerged by natural selection. In that case, traits are termed ‘exaptations’, a concept proposed by Stephen Jay Gould: in the same way that the nose can be used to perch spectacles on, a given brain module can be used to play chess. Smail then outlines the traditional viewpoint of evolutionary psychology, which has it that the 140 000 year history of hominins is too short to have influenced behavioural modules; that our brains are more suited to the East African savannahs than to industrialized society; and that human civilization entirely results from cultural, not biological evolution. As Sir Peter Medawar once put it: ‘We could return to the Stone Age in one generation’ (Medawar 1982). Ancient instincts from this ‘evolutionary hangover’ can still be identified, such fear of the dark, males being attracted to females younger than their actual partner and aversion to mating with persons one grew up with, even if they are unrelated. But subsequently Smail delicately dismantles the position that civilization put an end to biology. The persistence of behavioural ‘fossils’ depends on conjectural backward reasoning, all domesticated animals having undergone remarkable transformations in less than 10 000 years. The ability of most humans to synthesize lactase and the protection against malaria provided by the sickle-cell trait testify to the occurrence of gene-culture co-evolution. The genetic diversity (polymorphisms) within each ‘race’ and sex posits against stability. And, finally, human society may well be an equally valid source of selection pressure as the classical predator-prey relationship (an ‘evolutionary armsrace’ with a single species). ‘Substantial changes could have taken place in the human genome since the time of the Roman Empire’, Smail wagers. In other words, Churchill’s brain may well have differed substantially from Cicero’s! The last chapter is a sobering dissection of recent cultural evolution, in which the author argues that, from the 18th Brain (2008), 131, 2798 ^2801 2799 century onwards through pressures of political and religious dominance and subservience, secretion of nerve transmitters has to some extent been replaced by a ‘dizzying array of mood-altering practices and substances’, from amusement (‘teletropy’) to gossip or cocaine (‘autotropy’). Overall, the text is elegantly written as well as accessible: lapses into historical jargon are few and far between. Apt metaphors reflect digestion of a wealth of knowledge about biology and evolution. The notes have been relegated to the back of the book, integrated with an impressive bibliography, while the index is excellent. Eighteenth century Europe inspires Smail to write: ‘. . . with its caffeinated culture, its sentimental novels and pornographic works, and its growing array of consumer goods, [it] provides a gold mine of case studies that could benefit from the adoption of neurohistorical perspectives’. The book edited by Whitaker, Smith and Finger, however, addresses cultural, not biological evolution. Indeed, the 18th century represents a crucial episode in history—to a large extent coinciding with the Enlightenment. That simple term represents a huge and multi-faceted transformation of society in general, in which the traditional authority of aristocrats and ecclesiasts was challenged by an emerging middle class, hungry not only for power, sometimes even revolution, but also for knowledge. The intellectual climate changed accordingly. Aristotelian views of the world and its inhabitants as an unmovable and coherent system, adorned with a Christian varnish by Thomas of Aquino and other church fathers, were gradually replaced by the urge to unravel the secrets of the natural world. The humanistic outlook of the philosophical vanguard verged on atheism (Israel, 2001), while local tongues replaced Latin as the language of science; human rights were to some extent bought at the price of a return to provincialism, one might say. And in medical thinking the body moved to the centre of attention, at the expense of the soul (Porter, 2003). The inevitable conflicts raged even within the minds of pioneers and caused Swammerdam and Stensen to return to the safe haven of religion; Stensen ended his life as a bishop in Rome. Diseases had until then been traditionally explained in humoral terms. Naturally, the Renaissance had prompted changes in Hippocratic and Galenic models of disease as a specific disturbance of the delicate equilibrium between essential body humours. Chemical and physical principles were included, such as fermentation, acid–base equilibrium and early particle theory. Nevertheless, the perception of normal and disturbed body functions remained essentially ‘fluidist’ until introduction of systematic post-mortem studies in the 18th century identified changes in defined organs as the substrate as well as the cause of disease. From then on medicine became ‘solidist’. Morgagni (1682–1771) rightly stands out as the father of pathological anatomy, by dint of his monumental book ‘De sedibus et causis morborum’ (‘about the seats and causes of diseases’), summarizing a lifetime’s experience of autopsy studies, 2800 Brain (2008), 131, 2798 ^2801 mostly performed in Padua. Of course change was in the air in 1671, when—in his 80th year—Morgagni’s work appeared. Yet the apparently simple term ‘seats’ encapsulates the immense paradigm shift that overturned medicine in the 18th century, from a ‘systems approach’ to an ‘organ-based approach’. From organs the attention would shift to tissues, from tissues to cells, from cells to DNA, and from DNA to proteomics. This is where the reductionist trajectory ends today, leaving us short-sightedly wondering how to reconstruct the system from a mass of details. But that is another story. The transformation of physiological and medical thinking in the 18th century forms the backdrop against which new ideas about the function of the nervous system emerged. In the multi-author book by Whitaker and colleagues that decor is alluded to but not explained, apart from a single chapter about the Gentlemen’s Magazine, which exemplifies the dissemination of knowledge across the middle classes. Most developments in neuroscience are distributed over the other 24 chapters. The editors have been rather liberal in their time scale, conveniently extending the ‘long 18th century’ from 1664 (Thomas Willis’ ‘De Cerebri Anatome’) to the 1840s (Emil Du Bois Reymond’s discovery of the action potential). The attempt to arrange the different contributions in a more or less thematic fashion has been only partly successful, as the chosen themes are somewhat nebulous, inviting overlap: ‘introduction’ (fine, with an excellent ‘neurocalendar’), ‘background’ (with surprisingly little about society, science or even medicine in general), ‘the nervous system’, ‘brain and behaviour’, ‘medical theories and applications’ and finally ‘cultural consequences’. Also the editorial introductions to each of the resulting six sections read more like summaries than syntheses. Although the information contained in the book is priceless, readers are left with the task of reconstructing the overall image for themselves. On the other hand, by choosing such an eclectic approach, the editors have remained true to their subject, since compilation as a manner of presenting facts is a hallmark of the Enlightenment. In that era reading became an active rather than a passive process, according to the inductive view that an encyclopaedic collection of separate, accurate observations would necessarily lead to the emergence of more general rules. Let me, then, try to paint the overall picture. The three conceptual leaps, more or less in consecutive order, as I would prefer to distinguish them in the growing body of knowledge concerning the nervous system in the 18th century, are: first, the notion that the cerebral substance and not the cerebrospinal fluid is the substrate of sensation, motion and cognition; second, that nerves conduct signals not by means of fluid or mechanical impulses, but through some mysterious ‘change’ and the ‘energy’ for inducing movement, sensation and thought resides only in the central nervous system, not in muscles or other peripheral tissues; and third, electricity proves to be the elusive force Book Review underlying the signalling process. Of course the story does not end there. But electrophysiology and localization of some defined functions in the brain are typically 19th and 20th century issues, while the problems of charting the innumerable networks and understanding consciousness still remain to be solved. The question of brain substance versus brain fluid as the substrate of mental activity receives surprisingly little attention in the book. True, conventional chronology has it that the ancient Greek notion of the cerebral ventricles as the seat of the mind was superseded by the middle of the 17th century, to a large extent through the teachings and writings of Sylvius De la Boë in Leiden and Willis in Oxford (Clarke and Dewhurst, 1996). But the analogy between blood as the life force of the body and cerebrospinal fluid as the medium of thought was too powerful to be dispelled overnight. Rene Descartes, whose ‘De homine’ was written in the 1630s but appeared only post-humously, in 1662, attributed a central role to cerebrospinal fluid as the medium through which signals are transmitted from the pineal gland to pores in the brain mantle and vice versa. Similar views lingered until the very end of the 18th century, which saw the publication of Sömmerring’s ‘Das organ der Seele’ (1796), a work that surprisingly receives no mention from Whitaker and colleagues. Sömmerring’s famous and accurate illustration of a sagittal section of the brain is accompanied by a multitude of citations leading him to conclude that the brain substance only serves to interact with the cerebrospinal fluid, which is the true ‘organ of mind’. The monograph closes with an epilogue by an aged Immanuel Kant (1724–1804), who wisely prefers to remain on the fence. Even though ‘solidist’ views on brain function largely prevailed in the 18th century, brain fluid was for a long time still held responsible for the transmission of signals through nerves. Of course this required nerves to be hollow, a view to which both Descartes and Willis subscribed. That sectioned nerves failed to show a lumen only led to the qualification that the canals through which the ‘animal spirits’ percolated should be very tiny. Theory has fooled the greatest observers, even Vesalius when, at least in the first edition of his Fabrica (1543), he hesitated to contradict Galen’s view on the passage of blood through the interventricular septum of the heart: ‘we are driven to wonder at the handywork of the Almighty by means of which the blood sweats from the right into the left ventricle through passages which escape human vision’. John Hunter (1728–93), actually a great experimentalist (Moore 2005), offered a theoretical counterargument against the thesis of nerves being hollow tubes: ‘nothing material is conveyed from the brain by the nerves, nor vice versa from the body to the brain; for if that was exactly the case, it would not be necessary for the nerves to be of the same materials with the brain . . .’. Eventually the existence of canaliculi was disproved experimentally, among others by Monro primus Book Review (1698–1767) in Edinburgh, confirming 17th century observations such as microscopical sections of a bovine optic nerve by Leeuwenhoek (1632–1723), and physiological studies with nerve–muscle preparations by Borelli (1608–79) and Swammerdam (1637–80). Alternative explanations were wanting, but some came close. Hartley (1705–57) postulated ‘particular vibrations’ in nerves as well as in the white matter of the brain, probably inspired by Newton’s physics but not in the sense that he assumed an analogy with musical strings. Bonnet (1720–93), eponymously remembered through the description of the syndrome of visual hallucinations in his partially blind maternal grandfather, chose the term ‘movements’ for a similarly corpuscular view of signal propagation without transportation, within and between ‘nerve fibres’—fibre being more a theoretical construct than a microscopical structure according to present connotations. At the same time, much debate revolved around the question of ‘irritability’, an older term revived by the Swiss physician Haller (1708–77), who thereby evoked a controversy with philosophical and even religious undertones. Irritability of muscle tissue was its capability of contracting through pricking, stretching, applying acrid substances and especially by ‘a torrent [current] of electrical matter’. Haller concluded that muscle harboured an intrinsic force (vis insita), independent from its nerves. This mechanical perception of muscle as a decentralized energy store was fiercely opposed by Robert Whytt (1714–66), a Scot who, like Haller, had studied with Boerhaave in Leiden. Whytt maintained, mainly through theoretical reasoning, that a ‘sentient principle’ transmitted by the brain, spinal cord and nerves was necessary as well as sufficient to explain muscular contraction. He also postulated the existence of a primary, immaterial principle governing motions and actions, but did not go so far as the animist position that the soul resides in every part and organ of the body. The present-day author of one of the two chapters on the issue considers the contest a tie; indeed Haller never attributed true autonomy to muscle. Electricity, a phenomenon (re)discovered by Cardano (1501–76) and christened by Gilbert (1544–1603), emerged as the solution to the riddle of nervous transmission towards the end of the 18th century. An early line of research was the study of electrical fish. Despite long-standing interest in the shocks transmitted by these animals it was still undecided whether they were mechanical or electrical in nature. In 1772, John Walsh (1726–95), a wealthy gentleman with an interest in natural history and a typical exponent of the Enlightenment, journeyed to La Rochelle to study torpedoes. On his return, Walsh struck up a collaboration with Hunter and Cavendish (1731–1810), by which the existence of animal electricity was confirmed beyond doubt—they even managed to store it in Leiden jars. The discovery of electricity in ‘ordinary’ nerves is traditionally situated in 1786, when Galvani (1737–98) hung some fresh frog legs on brass hooks from the iron railings in his garden. His initial explanation Brain (2008), 131, 2798 ^2801 2801 was ‘fluidist’, in that he assumed secretion of an electrical substance by the brain, an antiquated notion that the physicist Volta (1745–1827) lost no time in attacking. It is from this starting point that electrophysiology took off in the next century. These are, in brief, the main developments that can be extracted from the compilation of individual essays gathered in Brain, Mind and Medicine. Other chapters describe the first inklings of cerebral localization (Pourfour du Petit, Bonnet, Swedenborg), evolving ideas about apoplexy, crazes about electrical treatments, and, unavoidably, dualism versus materialism. Gaps and overlaps are inevitable in multi-author books, but the index might have been more helpful: words such as ‘science’ and ‘nerve’ receive hordes of citations, while one looks in vain for some persons, even if repeatedly mentioned in the text (e.g. Pivati and Ingenhousz). Some authors indulge in footnotes, while others introduce secondary citations—almost anathema in an historical treatise. The two books differ not only in content but also in execution. Smail single-handedly tells a complicated though at the same time compelling story about evolution and the brain in 202 pages, notes excluded. Despite excursions on byroads and the ushering in of other authors, the reader never gets lost. The 379 double columns of the multiauthor book on 18th century neuroscience provide a wealth of information, but in the form of a Diderot-like compilation from which the reader has to reconstruct the main story. What the two books have in common other than the brain as subject matter is that the authors venture in foreign territory. The historian Smail valiantly enters an arena where evolutionary biologists were already engaged in bitter feuds. The scores of authors contributing bits and pieces of 18th century neuroscience are for the most part not historians, but physicians, psychologists, basic scientists or philosophers. Both books are laudable attempts to bridge Lord (CP) Snow’s ‘two cultures’, humanities and science, a task becoming increasingly demanding as fragmentation of knowledge continues. Flak from specialists will not be wanting, but often the soil is most fertile in border zones between disciplines. Jan van Gijn University Medical Centre Utrecht, The Netherlands Advance Access publication September 19, 2008 doi: 10.1093/brain/awn210 Clarke E, Dewhurst K. An Illustrated History of Brain Function - Imaging the Brain from Antiquity to the Present. San Francisco: Norman; 1996. Israel JI. Radical Enlightenment. Oxford: Oxford University Press; 2001. Medawar PB. Does ethology throw any light on human behaviour? In: Pluto’s Republic. Oxford: Oxford University Press; 1982. p. 191–202. Moore W. The Knife Man: The Extraordinary Life and Times of John Hunter, Father of Modern Surgery. London: Bantam Press; 2005. Porter R. Flesh in the Age of Reason. London: Allen Lane; 2003. Sömmerring ST. Über das Organ der Seele. Königsberg: Friedrich Nicolovius; 1796.