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Cortex Cerebri. Performance, Structural and Functional Organization of the Cortex
B OO K
R EV I EWS young children reveals that, whereas human toddlers and preschoolers seem to develop a system for interpreting each others’ (and their own) behavior in mentalistic ways, chimpanzees might be doing neither3–5,7. Thus, although chimpanzees are masters at using each others’ gaze to discover things not in their immediate visual field, every method we have developed to ask them, do you understand that vision is about (or refers to) something?, they have unselfconsciously replied, ‘no’3. This discovery of an apparent dissociation between sophisticated gazefollowing and an appreciation of the mental state of attention behind gaze, raises troubling questions. On the one hand, it raises the question of whether the behaviors Baron-Cohen cites as evidence of shared attention in 9- to 18-month-olds (that is, pointing, gaze-following, gaze-alternation), are really an indication of an understanding of the mental state of attention. If apes follow your gaze without appreciating the attentional states behind it, so too might human infants. However, it is possible that we need to be prepared to think differently about certain behaviors depending on whether apes or human infants are displaying them. Perhaps when apes engage in ‘shared attention’ behaviors they do not understand them in a mentalistic fashion, but when human infants engage in the exact same behaviors they do. Before we are attacked for creating a double-standard, consider the following. Might it not be the case that gaze-following, deception, and the like are fairly ancient behavioral mechanisms which evolved long before anything like SAM or ToMM were in place? Perhaps it is our species alone that has specialized in representing each other’s mental states, and in doing so have been placed in the unique position of being able to reinterpret ancestral behavioral patterns, which evolved long before humans appeared on the scene3. For example, after following someone’s gaze, when is it, exactly, that humans wonder what it is they are looking at? Does our behavior follow from the mentalistic query, or is it exactly the reverse? We suspect that much of the social value of theory of mind occurs in
exactly this retrospective way – as a means for planning future social action, not as a means of solving on-line social problems. To put the point directly, whereas BaronCohen (and others) tend to describe social creatures as needing a powerful theory of mind in the thick of social situations (pp. 23–30), we envision nearly the opposite: what they need most is a means of quickly selecting the appropriate behavioral script in order to act rapidly. Theory of mind is an added bonus. Thus, in humans there appears to be a connection between an expression of certain behaviors and at least a retrospective mentalistic interpretation of them. However, this connection might reflect the operation of evolutionary innovations peculiar to our species, which now develop alongside more ancestral behaviors that were originally unconnected with an understanding of mental states. Two versions of this possibility exist. First, humans might start off on a different track altogether, so that during each step of cognitive development an interpretative mechanism related to theory of mind allows for a qualitatively different kind of understanding of behavior than that which is present in most other species. In this case, the evolutionary innovation in theory of mind was woven into the early portions of the ancestral cognitive developmental pathways. A second possibility is that the behaviors that Baron-Cohen and others see as evidence that 9-month-old infant humans engage in ‘shared attention’ or ‘intentionality detection’, are in truth supported by no more than clever behavioral algorithms. It might be that rather than meddling with the earliest portions of the shared cognitive pathways of great apes and humans, evolution has woven in a theory-of-mind system at later stages. For example, it is quite compatible with a sceptical view of the developmental literature in this area that human infants must await their second year of life before they develop the evolutionarily novel cognitive structures that allow them to move from a state of ‘mindblindness’ to a vantage point from which they can see the behavior of themselves and others in genuinely mentalistic terms.
Cortex Cerebri. Performance, Structural and Functional Organization of the Cortex by O.D. Creutzfeldt, Oxford Science Publications, 1995. £65.00 (xiv + 658 pages) ISBN 0 19 852324 6 I remember clearly when Otto Creutzfeldt showed me his newly completed edition of Cortex Cerebri, in what must have been 1983. That was, of course, the original German version, and I remember suggesting that an English version would be a sure 300
TINS Vol. 19, No. 7, 1996
success. I did not know that an English version was almost ready in 1985, as Mary Creutzfeldt tells us in her Preface to this, that finally finished version. In the early 1980s this book represented a superb account of what we knew
Much of what we have said is compatible with many of Baron-Cohen’s ideas. However, this view does mean that we need to seriously rethink the evolutionary approach Baron-Cohen adopts to the problem at hand. Evolution will be of very little heuristic help if we are content to say, ‘it exists, therefore it must have evolved.’ If theory of mind is largely absent in such social species as chimpanzees and other non-human primates, then what does the Machiavellian Intelligence hypothesis really contribute to our understanding of the evolutionary history of mindreading? For that matter, even if our ongoing research ultimately reveals aspects of a limited mindreading system in chimpanzees, what about the many other social mammals and insects for whom the ‘contingency stance’ might work just fine? To be sure, we can imagine how theory of mind might be useful in social situations, but if most social organisms have no theory of mind then how can we offer sociality as an explanation for its evolution? Exactly how social a creature need you be to evolve SAM or ToMM? What is it about group-living per se that has driven the evolution of various aspects of theory of mind? Although Baron-Cohen certainly does not purport to answer these questions, his fascinating excursion certainly sets the stage for asking them. Daniel J. Povinelli Theodore J. Povinelli Laboratory of Comparative Behavioral Biology, University of Southwestern Louisiana New Iberia Research Center, 4401 West Admiral Doyle Drive, New Iberia, LA 70501, USA. References 1 Fodor, J. (1983) The Modularity of Mind, MIT Press 2 Baron-Cohen, S., Leslie, A. and Frith, U. (1985) Cognition 21, 37– 46 3 Povinelli, D.J. and Preuss, T.M. (1995) Trends Neurosci. 18, 418– 424 4 Povinelli, D.J. and Eddy, T.J. (1996) Monogr. Soc. Res. Child Dev. 61 (3, Serial No. 247) 5 Povinelli, D.J. and Eddy, T.J. Psychol. Sci. (in press) 6 de Waal, F.B.M. (1982) Chimpanzee Politics, Harper and Row 7 Tomasello, M. and Call, J. (1994) Yearbook Phys. Anthropol. 37, 273–305
about the cerebral cortex, and it is a pity that it was inaccessible to most, unless their German was adequate. Otto Creutzfeldt himself contributed so much to that fount of knowledge, and his students and their students are now continuing that tradition. Although he was internationally renowned for his single-unit electrophysiological studies on the mammalian visual system, including the cortex, his collaboration with others, including even anatomists, ensured that he had a
Copyright © 1996, Elsevier Science Ltd. All rights reserved. 0166 - 2236/96/$15.00
PII: S0166-2236(96)60018-6
B OO K wide understanding of the problems and achievements in other fields. Indeed, in his Preface to the 1983 edition he emphasizes the importance of taking structural and functional considerations together. His inspiration for the book came, I believe, from the fact that details about the cortex had tended to be written as the last part of a description about a specific system, such as the visual system, and he wanted to make the cortex stand in its own right. That the original version was in German has a historical basis, as it begun as a chapter in a German textbook, but the real reasons are deeper than this and reflect Otto’s background and character. Perhaps this is why we have had to wait so long for the English version. But another reason is because of his attention to detail and, I strongly suspect, his not wanting to publish anything that did not meet his strict criteria for completeness and excellence. The result was that he never finished the translation and we must congratulate Mary for taking on the task and completing it. The book starts with a brief historical introduction that serves to put the situation regarding the cortex in the 1980s in perspective. It is indeed very brief, but perhaps that gives an idea of Otto’s view of the comparative infancy of the subject at that time. A chapter on phylogenetic and ontogenetic aspects of the cortex follows, again admirably brief but eminently readable. However, it is clear that we are reading the situation as it was a few years ago, as can only be expected.
In the excellent Chapter 3 on cortical structure we find ourselves back to the early twentieth century, not in any pejorative sense, but rightly emphasizing the work of classic neuroanatomists such as Brodmann in setting us on the right path as far as cortical localization is concerned. Although old, this is topical stuff. This chapter continues with descriptions of neurones and their afferent and efferent projections, and glia. Remarkable descriptions for the time, they feel a little incomplete now, even after the revision in 1989 from which most of the book benefited, but they still serve to mark what is enduring in the topic, without venturing to give excessive details on the ‘very’ new and, possibly, ephemeral. A surprise to me is that ‘neurone’ has the second ‘e’. That was how I used to spell it until Otto told me to change, as that form was wrong, not reflecting the Greek! No compromise was possible. But, as you see, this journal does not follow Otto’s advice! The next two chapters enter into Otto’s very special domain, that of neurophysiology, and one must not forget that he was responsible for actually doing so much of what is written in this book, either himself or through his students and collaborators. It is pointless to describe these writings here: they must be read. Then there follow two chapters on the sensory, motor and association cortices, which bring together the points that Otto considered to be significant in them, and this emerges as an encyclopaedia of knowl-
Autoimmune Neurological Disease by Michael P. Pender and Pamela A. McCombe, Cambridge University Press, 1995. £55.00 (377 pages) ISBN 0 521 46113 8 It has been said that ‘neurologists know a lot but can do very little, neurosurgeons know very little but do a lot, and neuropathologists know everything – but by then it’s too late’. This pessimism is being undermined by the increasing evidence for immunopathogenic mechanisms in some neurological conditions, and successful treatments based on this knowledge. This two-author book covers these developments and the clinical features of most of the known autoimmune neurological disorders, including ‘paraneoplastic’ disorders which are secondary to cancer in other tissues, and their animal models. The contents illustrate the great specificity with which the immune system can recognize individual neuronal proteins once selftolerance is broken. The nature and strength of the evidence for autoimmunity in a particular disease varies widely for different diseases. Multiple sclerosis (MS) is associated with
lymphocytic infiltrates, loss of oligodendrocytes, demyelination and gliosis in the CNS. Expression of major histocompatibility complex class II molecules (on macrophages and astrocytes) is increased and CD4+ T cells are found in acute MS lesions. B-cell activation is evidenced by the presence of oligoclonal bands in the cerebrospinal fluid. Furthermore, the similarity of MS to the animal model, experimental autoimmune encephalitis (EAE), which develops following immunization with myelin antigens (myelin basic protein or proteolipid protein), and the presence of T cells reactive to myelin basic protein in MS patients provides circumstantial evidence for an autoimmune pathogenesis. However, it is not known whether the antigen-specific T cells are the primary cause of the disease, or reflect secondary sensitization to antigens exposed during demyelination from some unidentified primary event.
Copyright © 1996, Elsevier Science Ltd. All rights reserved. 0166 - 2236/96/$15.00
edge, perhaps again missing the very latest on the subject but providing us with an immediate grasp of what was important, and will remain important. There is not much speculation here: just solid information, and that is what we need! The last three chapters deal with ‘higher’ cortical functions (cognition, limbic activity, and a final more speculative section on defining cortical ‘function’, including mind and reason). Here the mind of the author is at last allowed a freer rein and meanders over the almost imponderable in our science. All the way through, I felt Otto’s rigid discipline, but he provides much food for thought. This book is compulsory reading for all in neuroscience research, and those coming into it. It is history, written by one who helped make that history. But it is much more than that: it points to where we have to go next. I am sure that Otto would be pleased with how cortical neuroscience has progressed since he left us to get on with it without him. As I look at this book now, my strongest impression is of the pungent tobacco smoke that was an inevitable part of any encounter with Otto. Is it possible that the publishers have used some new technique to impregnate their printing paper, or is my Cortex Cerebri playing me up? Laurence J. Garey Dept of Anatomy, Charing Cross and Westminster Medical School, London, UK W6 8RF.
Even the pathogenic role of antibodies to specific proteins is not always clear. For example, the ‘stiff-man syndrome’, is a chronic condition in which disinhibition of upper motor neurones leads to simultaneous contraction of agonist and antagonist muscles resulting in severe muscle rigidity and painful spasms. About 50% of patients have antibodies to glutamic acid decarboxylase (GAD) that are restricted to inhibitory GABA-containing neurones (and pancreatic b cells); some others, notably those with an associated cancer, have antibodies to amphiphysin. It seems reasonable to suppose that a disease characterized clinically and electrophysiologically by excessive muscle contraction could be mediated by an immune response directed against a component of inhibitory neurones. It is more difficult to imagine the role that antibodies to amphiphysin (a component of the vesicular membrane in many different synapses) might play in this disease. In either case, the question arises as to how an immune response directed against cytoplasmic antigens of neurones that are supposed to be protected by the ‘blood–brain barrier’ can lead to neuronal
PII: S0166-2236(96)60017-4
TINS Vol. 19, No. 7, 1996
301
R E V I E WS
R EV I EWS young children reveals that, whereas human toddlers and preschoolers seem to develop a system for interpreting each others’ (and their own) behavior in mentalistic ways, chimpanzees might be doing neither3–5,7. Thus, although chimpanzees are masters at using each others’ gaze to discover things not in their immediate visual field, every method we have developed to ask them, do you understand that vision is about (or refers to) something?, they have unselfconsciously replied, ‘no’3. This discovery of an apparent dissociation between sophisticated gazefollowing and an appreciation of the mental state of attention behind gaze, raises troubling questions. On the one hand, it raises the question of whether the behaviors Baron-Cohen cites as evidence of shared attention in 9- to 18-month-olds (that is, pointing, gaze-following, gaze-alternation), are really an indication of an understanding of the mental state of attention. If apes follow your gaze without appreciating the attentional states behind it, so too might human infants. However, it is possible that we need to be prepared to think differently about certain behaviors depending on whether apes or human infants are displaying them. Perhaps when apes engage in ‘shared attention’ behaviors they do not understand them in a mentalistic fashion, but when human infants engage in the exact same behaviors they do. Before we are attacked for creating a double-standard, consider the following. Might it not be the case that gaze-following, deception, and the like are fairly ancient behavioral mechanisms which evolved long before anything like SAM or ToMM were in place? Perhaps it is our species alone that has specialized in representing each other’s mental states, and in doing so have been placed in the unique position of being able to reinterpret ancestral behavioral patterns, which evolved long before humans appeared on the scene3. For example, after following someone’s gaze, when is it, exactly, that humans wonder what it is they are looking at? Does our behavior follow from the mentalistic query, or is it exactly the reverse? We suspect that much of the social value of theory of mind occurs in
exactly this retrospective way – as a means for planning future social action, not as a means of solving on-line social problems. To put the point directly, whereas BaronCohen (and others) tend to describe social creatures as needing a powerful theory of mind in the thick of social situations (pp. 23–30), we envision nearly the opposite: what they need most is a means of quickly selecting the appropriate behavioral script in order to act rapidly. Theory of mind is an added bonus. Thus, in humans there appears to be a connection between an expression of certain behaviors and at least a retrospective mentalistic interpretation of them. However, this connection might reflect the operation of evolutionary innovations peculiar to our species, which now develop alongside more ancestral behaviors that were originally unconnected with an understanding of mental states. Two versions of this possibility exist. First, humans might start off on a different track altogether, so that during each step of cognitive development an interpretative mechanism related to theory of mind allows for a qualitatively different kind of understanding of behavior than that which is present in most other species. In this case, the evolutionary innovation in theory of mind was woven into the early portions of the ancestral cognitive developmental pathways. A second possibility is that the behaviors that Baron-Cohen and others see as evidence that 9-month-old infant humans engage in ‘shared attention’ or ‘intentionality detection’, are in truth supported by no more than clever behavioral algorithms. It might be that rather than meddling with the earliest portions of the shared cognitive pathways of great apes and humans, evolution has woven in a theory-of-mind system at later stages. For example, it is quite compatible with a sceptical view of the developmental literature in this area that human infants must await their second year of life before they develop the evolutionarily novel cognitive structures that allow them to move from a state of ‘mindblindness’ to a vantage point from which they can see the behavior of themselves and others in genuinely mentalistic terms.
Cortex Cerebri. Performance, Structural and Functional Organization of the Cortex by O.D. Creutzfeldt, Oxford Science Publications, 1995. £65.00 (xiv + 658 pages) ISBN 0 19 852324 6 I remember clearly when Otto Creutzfeldt showed me his newly completed edition of Cortex Cerebri, in what must have been 1983. That was, of course, the original German version, and I remember suggesting that an English version would be a sure 300
TINS Vol. 19, No. 7, 1996
success. I did not know that an English version was almost ready in 1985, as Mary Creutzfeldt tells us in her Preface to this, that finally finished version. In the early 1980s this book represented a superb account of what we knew
Much of what we have said is compatible with many of Baron-Cohen’s ideas. However, this view does mean that we need to seriously rethink the evolutionary approach Baron-Cohen adopts to the problem at hand. Evolution will be of very little heuristic help if we are content to say, ‘it exists, therefore it must have evolved.’ If theory of mind is largely absent in such social species as chimpanzees and other non-human primates, then what does the Machiavellian Intelligence hypothesis really contribute to our understanding of the evolutionary history of mindreading? For that matter, even if our ongoing research ultimately reveals aspects of a limited mindreading system in chimpanzees, what about the many other social mammals and insects for whom the ‘contingency stance’ might work just fine? To be sure, we can imagine how theory of mind might be useful in social situations, but if most social organisms have no theory of mind then how can we offer sociality as an explanation for its evolution? Exactly how social a creature need you be to evolve SAM or ToMM? What is it about group-living per se that has driven the evolution of various aspects of theory of mind? Although Baron-Cohen certainly does not purport to answer these questions, his fascinating excursion certainly sets the stage for asking them. Daniel J. Povinelli Theodore J. Povinelli Laboratory of Comparative Behavioral Biology, University of Southwestern Louisiana New Iberia Research Center, 4401 West Admiral Doyle Drive, New Iberia, LA 70501, USA. References 1 Fodor, J. (1983) The Modularity of Mind, MIT Press 2 Baron-Cohen, S., Leslie, A. and Frith, U. (1985) Cognition 21, 37– 46 3 Povinelli, D.J. and Preuss, T.M. (1995) Trends Neurosci. 18, 418– 424 4 Povinelli, D.J. and Eddy, T.J. (1996) Monogr. Soc. Res. Child Dev. 61 (3, Serial No. 247) 5 Povinelli, D.J. and Eddy, T.J. Psychol. Sci. (in press) 6 de Waal, F.B.M. (1982) Chimpanzee Politics, Harper and Row 7 Tomasello, M. and Call, J. (1994) Yearbook Phys. Anthropol. 37, 273–305
about the cerebral cortex, and it is a pity that it was inaccessible to most, unless their German was adequate. Otto Creutzfeldt himself contributed so much to that fount of knowledge, and his students and their students are now continuing that tradition. Although he was internationally renowned for his single-unit electrophysiological studies on the mammalian visual system, including the cortex, his collaboration with others, including even anatomists, ensured that he had a
Copyright © 1996, Elsevier Science Ltd. All rights reserved. 0166 - 2236/96/$15.00
PII: S0166-2236(96)60018-6
B OO K wide understanding of the problems and achievements in other fields. Indeed, in his Preface to the 1983 edition he emphasizes the importance of taking structural and functional considerations together. His inspiration for the book came, I believe, from the fact that details about the cortex had tended to be written as the last part of a description about a specific system, such as the visual system, and he wanted to make the cortex stand in its own right. That the original version was in German has a historical basis, as it begun as a chapter in a German textbook, but the real reasons are deeper than this and reflect Otto’s background and character. Perhaps this is why we have had to wait so long for the English version. But another reason is because of his attention to detail and, I strongly suspect, his not wanting to publish anything that did not meet his strict criteria for completeness and excellence. The result was that he never finished the translation and we must congratulate Mary for taking on the task and completing it. The book starts with a brief historical introduction that serves to put the situation regarding the cortex in the 1980s in perspective. It is indeed very brief, but perhaps that gives an idea of Otto’s view of the comparative infancy of the subject at that time. A chapter on phylogenetic and ontogenetic aspects of the cortex follows, again admirably brief but eminently readable. However, it is clear that we are reading the situation as it was a few years ago, as can only be expected.
In the excellent Chapter 3 on cortical structure we find ourselves back to the early twentieth century, not in any pejorative sense, but rightly emphasizing the work of classic neuroanatomists such as Brodmann in setting us on the right path as far as cortical localization is concerned. Although old, this is topical stuff. This chapter continues with descriptions of neurones and their afferent and efferent projections, and glia. Remarkable descriptions for the time, they feel a little incomplete now, even after the revision in 1989 from which most of the book benefited, but they still serve to mark what is enduring in the topic, without venturing to give excessive details on the ‘very’ new and, possibly, ephemeral. A surprise to me is that ‘neurone’ has the second ‘e’. That was how I used to spell it until Otto told me to change, as that form was wrong, not reflecting the Greek! No compromise was possible. But, as you see, this journal does not follow Otto’s advice! The next two chapters enter into Otto’s very special domain, that of neurophysiology, and one must not forget that he was responsible for actually doing so much of what is written in this book, either himself or through his students and collaborators. It is pointless to describe these writings here: they must be read. Then there follow two chapters on the sensory, motor and association cortices, which bring together the points that Otto considered to be significant in them, and this emerges as an encyclopaedia of knowl-
Autoimmune Neurological Disease by Michael P. Pender and Pamela A. McCombe, Cambridge University Press, 1995. £55.00 (377 pages) ISBN 0 521 46113 8 It has been said that ‘neurologists know a lot but can do very little, neurosurgeons know very little but do a lot, and neuropathologists know everything – but by then it’s too late’. This pessimism is being undermined by the increasing evidence for immunopathogenic mechanisms in some neurological conditions, and successful treatments based on this knowledge. This two-author book covers these developments and the clinical features of most of the known autoimmune neurological disorders, including ‘paraneoplastic’ disorders which are secondary to cancer in other tissues, and their animal models. The contents illustrate the great specificity with which the immune system can recognize individual neuronal proteins once selftolerance is broken. The nature and strength of the evidence for autoimmunity in a particular disease varies widely for different diseases. Multiple sclerosis (MS) is associated with
lymphocytic infiltrates, loss of oligodendrocytes, demyelination and gliosis in the CNS. Expression of major histocompatibility complex class II molecules (on macrophages and astrocytes) is increased and CD4+ T cells are found in acute MS lesions. B-cell activation is evidenced by the presence of oligoclonal bands in the cerebrospinal fluid. Furthermore, the similarity of MS to the animal model, experimental autoimmune encephalitis (EAE), which develops following immunization with myelin antigens (myelin basic protein or proteolipid protein), and the presence of T cells reactive to myelin basic protein in MS patients provides circumstantial evidence for an autoimmune pathogenesis. However, it is not known whether the antigen-specific T cells are the primary cause of the disease, or reflect secondary sensitization to antigens exposed during demyelination from some unidentified primary event.
Copyright © 1996, Elsevier Science Ltd. All rights reserved. 0166 - 2236/96/$15.00
edge, perhaps again missing the very latest on the subject but providing us with an immediate grasp of what was important, and will remain important. There is not much speculation here: just solid information, and that is what we need! The last three chapters deal with ‘higher’ cortical functions (cognition, limbic activity, and a final more speculative section on defining cortical ‘function’, including mind and reason). Here the mind of the author is at last allowed a freer rein and meanders over the almost imponderable in our science. All the way through, I felt Otto’s rigid discipline, but he provides much food for thought. This book is compulsory reading for all in neuroscience research, and those coming into it. It is history, written by one who helped make that history. But it is much more than that: it points to where we have to go next. I am sure that Otto would be pleased with how cortical neuroscience has progressed since he left us to get on with it without him. As I look at this book now, my strongest impression is of the pungent tobacco smoke that was an inevitable part of any encounter with Otto. Is it possible that the publishers have used some new technique to impregnate their printing paper, or is my Cortex Cerebri playing me up? Laurence J. Garey Dept of Anatomy, Charing Cross and Westminster Medical School, London, UK W6 8RF.
Even the pathogenic role of antibodies to specific proteins is not always clear. For example, the ‘stiff-man syndrome’, is a chronic condition in which disinhibition of upper motor neurones leads to simultaneous contraction of agonist and antagonist muscles resulting in severe muscle rigidity and painful spasms. About 50% of patients have antibodies to glutamic acid decarboxylase (GAD) that are restricted to inhibitory GABA-containing neurones (and pancreatic b cells); some others, notably those with an associated cancer, have antibodies to amphiphysin. It seems reasonable to suppose that a disease characterized clinically and electrophysiologically by excessive muscle contraction could be mediated by an immune response directed against a component of inhibitory neurones. It is more difficult to imagine the role that antibodies to amphiphysin (a component of the vesicular membrane in many different synapses) might play in this disease. In either case, the question arises as to how an immune response directed against cytoplasmic antigens of neurones that are supposed to be protected by the ‘blood–brain barrier’ can lead to neuronal
PII: S0166-2236(96)60017-4
TINS Vol. 19, No. 7, 1996
301
R E V I E WS