The Neurobiology of the Prefrontal Cortex: Anatomy, Evolution, and the Origin of Insight

422 Pages·2012·3.96 MB·English

by  Richard E. Passingham

The Neurobiology of
the Prefrontal Cortex
Oxford Psychology Series
Editors: Mark D’Eposito, Daniel Schacter, Jon Driver, Anne Treisman, Trevor Robbins,
Lawrence Weiskrantz
1. The Neuropsychology of Anxiety 26. Attention and Memory
J. A. Gray N. Cowan
2. Elements of Episodic Memory 27. The Visual Brain in Action
E. Tulving A. D. Milner and M. A. Goodale
3. Conditioning and Associative Learning 28. Perceptual Consequences of Cochlear
N. J. Mackintosh Damage
4. Visual Masking B. C. J. Moore
B. G. Breitmeyer 29. Binocular Vision and Stereopsis
5. The Musical Mind I. P. Howard and B. J. Rogers
J. A. Sloboda 30. The Measurement of Sensation
6. Elements of Psychophysical Theory D. Laming
J.-C. Falmagne 31. Conditioned Taste Aversion
7. Animal Intelligence J. Bures, F. Bermúdez–Rattoni, and
L. Weiskrantz T. Yamamoto
8. Response Times 32. The Developing Visual Brain
R. D. Luce J. Atkinson
9. Mental Representations 33. The Neuropsychology of Anxiety, 2e
A. Paivio J. A. Gray and N. McNaughton
10. Memory, Imprinting, and the Brain 34. Looking Down on Human Intelligence
G. Horn I. J. Deary
11. Working Memory 35. From Conditioning to Conscious Recollection
A. Baddeley H. Eichenbaum and N. J. Cohen
12. Blindsight 36. Understanding Figurative Language
L. Weiskrantz S. Glucksberg
13. Profile Analysis 37. Active Vision
D. M. Green J. M. Findlay and I. D. Gilchrist
14. Spatial Vision 38. The Science of False Memory
R. L. DeValois and K. K. DeValois C. J. Brainerd and V. F. Reyna
15. The Neural and Behavioural Organization of 39. The Case for Mental Imagery
Goal-Directed Movements S. M. Kosslyn, W. L. Thompson, and
M. Jeannerod G. Ganis
16. Visual Pattern Analyzers 40. Seeing Black and White
N. V. S. Graham A. Gilchrist
17. Cognitive Foundations of Musical Pitch 41. Visual Masking, 2eB.
C. L. Krumhansl Breitmeyer and H. Ö˘gmen
18. Perceptual and Associative Learning 42. Motor Cognition
G. Hall M. Jeannerod
19. Implicit Learning and Tacit Knowledge 43. The Visual Brain in Action
A. S. Reber A. D. Milner and M. A. Goodale
20. Neuromotor Mechanisms in Human 44. The Continuity of Mind
Communication M. Spivey
D. Kimura 45. Working Memory, Thought, and Action
21. The Frontal Lobes and Voluntary Action A. Baddeley
R. Passingham 46. What Is Special about the Human Brain?
22. Classification and Cognition R. Passingham
W. K. Estes 47. Visual Reflections
23. Vowel Perception and Production M. McCloskey
B. S. Rosner and J. B. Pickering 48. Principles of Visual Attention
24. Visual Stress C. Bundesen and T. Habekost
A. Wilkins 49. Major Issues in Cognitive Aging
25. Electrophysiology of Mind T. A. Salthouse
Edited by M. D. Rugg and M. G. H. Coles
The Neurobiology
of the Prefrontal
Cortex
Anatomy, Evolution, and
the Origin of Insight
Richard E. Passingham
Steven P. Wise
1
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Dedication
In memory of
Patricia S. Goldman-Rakic (1937–2003)
Edward V. Evarts (1926–1985)
Edward G. Jones (1939–2011)
Animals studied by Americans rush about frantically, with an incredible display
of hustle and pep, and at last achieve the desired result by chance. Animals
observed by Germans sit still and think and at last evolve the solution out of
their inner consciousness.
— Bertrand Russell, An Outline of Philosophy (1925)
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Preface
In the 1960s, the Russian neuropsychologist Alexander Luria gave a much anticipated
lecture in London, which one of us attended. He started by drawing a brain on the black-
board and placing a large question mark over the prefrontal cortex. At the end of the
lecture, he triumphantly rubbed out the question mark. Readers of this book will not be
so lucky.
Why prefrontal, why now?
One of us had a go in an earlier book, The Frontal Lobes and Voluntary Action (Passingham
1993). That book treated the frontal lobes as a whole, including its motor areas, and it
suggested that their key functions involve conditional behaviour. In this kind of behav-
iour, one sensory context determines which action to take and other contexts lead to
other actions.
The publisher later asked for a second edition, but a simple revision was out of the
question. Too much has changed. The 1993 book appeared in the infancy of functional
imaging, which has altered the field profoundly. The book proudly showed a brain scan
as the frontispiece and described the first author’s early results from positron emission
tomography — and that was all. The intervening years have seen thousands of imaging
papers, with more on the prefrontal cortex than on anything else.
Two other major advances have also changed the field. First, neuropsychological stud-
ies in monkeys have experienced a renaissance. Recent studies differ from earlier ones in
their use of more sophisticated experimental designs, which often focus on advanced
cognition. Second, neurophysiological studies in monkeys have matured considerably,
and for similar reasons. Neurophysiologists can now address the advanced cognitive
capacities that epitomize primate behaviour. They do so with a broader array of tasks, and
better control conditions, than anyone imagined in 1993.
S o what follows is a new and different book, and not a second edition. We decided to
write it because we have retired from laboratory research. One of us doesn’t like garden-
ing, and the other tends a very small one. We decided to write the book together because
both of us have thought and written about the prefrontal cortex for some time now, and
neither of us believes that our previous contributions provide a satisfactory solution to
the problem.
A comparative approach
As readers might gather from what we have said so far, this book relies heavily on monkey
research. But this does not mean that we ignore advances that have come from imaging
in healthy people or from studies of patients. Indeed, we make extensive use of them. But
in doing so, we interpret these advances in the light of the knowledge gained by studying
other primates.
viii PREFACE
We recognize that many neuroscientists proceed without using this knowledge and that
they do so very successfully. Cognitive psychologists do not, as a rule, concern themselves
with the details of research on monkeys, and they have advanced our knowledge consid-
erably. Likewise, the bulk of imaging research makes little use of what we know about
other primates, and the field continues to prosper. However, it seems to us that in using
imaging to explore the vast array of human abilities, one may fail to appreciate a simple
fundamental function that ties everything together. The comparative perspective that
comes from studying other primates can help us see the big picture.
O ur comparative approach also explains the title of this book. We place what we know
about the prefrontal cortex in an evolutionary perspective. This seems to us to be more
like neurobiology than like standard neuroscience or neuropsychology. And so we call the
book The Neurobiology of the Prefrontal Cortex .
T he epigraph of this book reflects our comparative slant, as well (p. v). Russell (1925)
was contrasting the studies of rats and cats by American psychologists such as Thorndike
(1898) with the studies of chimpanzees by Germans such as Köhler (1925). Thorndike
stressed a general-purpose, reinforcement mechanism for learning by trial-and-error.
The trouble with trial-and-error learning is that it is resigned to many errors, and espe-
cially so in unusual circumstances. In this book, we claim that primates do not come to
each new situation afresh. Instead, they swiftly and extensively transfer what they have
learned to novel and rare situations. This is the insight of which Kohler wrote, and we
believe that it depends upon the prefrontal cortex.
Style and terminology
We have chosen a style that contrasts with a typical academic monograph in several ways.
This book makes no effort to achieve comprehensive coverage or to recount the history
of the field. Several thousand papers are published on the prefrontal cortex each year. We
could not write, and no reader could tolerate, a comprehensive review. So we engage
unapologetically in cherry-picking evidence to advocate a position. We realize the danger
of this approach: one can easily ignore contrary evidence and so create the illusion of clar-
ity where none exists. But we find it preferable to an exhaustive review that leaves readers
exhausted — but none the wiser.
Everyone seems to have their own language for discussing the prefrontal cortex. So
some brief notes about terminology might prove helpful:
◆ W e use some convenient but loose terms. When we use the word animals we mean
nonhuman animals, and by monkeys we mean macaque monkeys, unless otherwise
stated. We also know that some people object to the phrase great ape, but we suspect
that readers will know what it means. We mean no disrespect to lesser apes, which we
hold in high esteem.
◆ We use the anatomical terms caudal and posterior interchangeably. These terms are
not, strictly speaking, synonymous, especially in humans, but they are close enough
for our purposes. Likewise for rostral and anterior. We also adopt the phrase g ranular
prefrontal cortex , although we know that its anatomy is not truly granular, as the pri-
mary sensory areas are.
PREFACE ix
◆ Much of the book relates results from experimental lesions. For convenience, we use
the term lesion to cover all kinds of procedures that prevent a cortical area from func-
tioning normally. These techniques include surgical removal, cell death due to excito-
toxic agents, inactivation with inhibitory transmitters or cooling, optogenetic methods,
and disruption of function by magnetic or electrical stimulation.
◆ In another convention, we use the term activity to describe the rate of neuronal action
potentials, commonly known as firing, discharge, modulation, or spiking, but we use
the term a ctivation to describe results from imaging experiments, mainly from func-
tional magnetic resonance imaging (fMRI). Chapter 1 explains why.
◆ We use the term i maging when the context makes it clear that the study measures acti-
vations, usually with fMRI, as opposed to structural imaging.
◆ We use several abbreviations, which are listed after the acknowledgements. Where we
think that the reader might need reminding of the unabbreviated form, we spell it out
again from time to time.
◆ The glossary explains selected terms from psychology and biology.
◆ After the preface, we use the abbreviation PF for prefrontal cortex throughout the
book.
◆ When we refer to regions within the prefrontal cortex, we usually do so by placing the
regional name before PF, as in orbital PF cortex. Occasionally, when the regional
descriptors get too long, we shorten them or use other abbreviations, such as OFC for
the orbital frontal cortex.
◆ Finally, like many people of our age, we persist in using the word subjects rather than
participants to describe people who take part in experiments. It seems to us that only
editors object to this, not the subjects themselves. We hope that no one feels subju-
gated as a result.