The evolution of memory systems : ancestors, anatomy, and adaptations

517 Pages·2017·6.29 MB·English

by  Graham

The Evolution of 
Memory Systems
Advance Praise
for The Evolution of Memory Systems
Capitalizing on major advances in our understanding of both memory and brain evolution,
this book provides the first – and long overdue – account of memory systems placed in an
evolutionary context. The result is a captivating and comprehensive survey of two histories,
the history of the brain and the history of ideas about memory, which culminates in a new
and provocative proposal for the origin of memory. Anyone interested in the brain and
behaviour, evolution, or the history of science will find The Evolution of Memory Systems a
stimulating read.
Morgan Barense, Associate Professor and Canada Research Chair in Cognitive Neuroscience,
Department of Psychology, University of Toronto, Canada
The authors convincingly demonstrate that memory systems, and perhaps all neural systems,
are best understood in terms of when and why they evolved to meet challenges of the past.
Thus, this is a book for those interested in how brains work, and how they differ. This impres-
sive book is like no other in its scope on the successive evolution of memory systems from
early vertebrates to present-day humans. I want all my students and co-workers to read it.
Jon H. Kaas, Distinguished Centennial Professor of Psychology, Vanderbilt University, USA
A critical component of defining who we are requires an understanding of our individual
past experiences and how they are represented in the brain, as well as how our brain, and in
particular memory circuits, evolved in mammals. This book is a tour-de-force on the evolu-
tion of memory systems in mammals. It provides a wonderful historical perspective, and an
extensive comparative analysis. While the major thrust is to understand human capabilities,
particularly circuitry involved in memory, the authors painstakingly review the literature and
clearly articulate that these systems did not evolve de novo in humans, but that a basic plan
was present in our earliest ancestors. This type of discussion is rarely found in a neuroscience
community entrenched in studies of single animal models. Kudos to the authors for writing
the most comprehensive and interesting text currently available on this topic.
Leah Krubitzer, MacArthur Fellow, Professor of Psychology, Center for Neuroscience,
University of California, Davis, USA
Through their combined evolutionary and neuroscience approach the authors beautifully
reveal the building blocks of memory systems that combine to produce the complexities of
cognition in the human brain.
Trevor W. Robbins CBE, Professor of Cognitive Neuroscience and Experimental Psychology,
University of Cambridge, UK
This is an important book for several reasons. First, there is the unique way that the authors
formulate their proposals within an evolutionary context, explaining what makes memory
special in mammals, in primates, and in humans. Second, their survey of the cognitive
neuroscience of memory is guided by an exciting and provocative new taxonomy of memory
systems that takes the reader far beyond the hippocampus and medial temporal lobe.
Matthew Rushworth, Professor of Cognitive Neuroscience, Department of Experimental Psychology,
University of Oxford, UK
The Evolution
of Memory Systems
Ancestors, anatomy,
and adaptations
Elisabeth A. Murray
Steven P. Wise
Kim S. Graham
1
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To our ancestors,
academic and anthropoid alike

Preface
Conception
This book began its life in the back seat of a car, as lives on occasion do. The second
author, then a graduate student, accompanied Mort Mishkin and Ted Jones on a quick
ride through the campus of Duke University. It was April 1977, and they had to hustle to
a symposium somewhere. As the graduate student sat silently in the back seat, Mishkin
spoke with building excitement about the famous amnesic patient, H.M. Jones seemed
mildly interested, but the graduate student could not have been more enthralled. As an
undergraduate he had attended a lecture on H.M., which fertilized a lifelong interest in
this seminal clinical case.
During the car ride, Mishkin declared that he had solved a longstanding mystery about
H.M. For decades, neuropsychologists had tried and failed to replicate H.M.’s memory
impairment in monkeys. In 1977, Mishkin thought he had finally done it by making a
lesion that included both the amygdala and the hippocampus. Given what little the gradu-
ate student knew about the brain and its evolution, the combination of these two struc-
tures seemed odd, but intriguing. At first glance, they did not appear to compose a natural
pair. Why, he wondered, would the amygdala and hippocampus hook up in the service of
memory, in some sort of exclusive relationship? All the same, a book on the evolution of
memory might arouse some interest, he thought, provided that Mishkin’s idea stood the
test of time. It didn’t, but the germ of the book survived in frozen form.
In the interim, the first and third authors studied memory systems intimately, while
the second author watched from the back seat, much as he did on that long- ago car
ride. Despite undeniable progress in understanding memory systems, no one— even to
this day—h as successfully placed them in an evolutionary context. Clearly, we would
understand memory systems better if we knew when they evolved and the selective pres-
sures that produced them. In 1977, however, and for decades thereafter, brain evolution
seemed more mysterious than memory systems would ever be. Slowly, that changed.
Neuroscientists now understand brain evolution much better than anyone could have
imagined back then. So, after nearly four decades of gestation, it seems like a good time to
deliver a book on the evolution of memory systems.
Scope
Although this book considers other species, it emphasizes primates. Not only are all the
authors primates, but our proposals depend on the idea that many cortical areas evolved
in our order. Readers who view the cortex of other mammals as replicas in miniature or
viii PrEfAcE
amalgams of primate areas will find our principal thesis unpalatable, to say the least. In
Chapter 2 (“New cortical areas”)* we summarize some of the evidence supporting our
view, but we recognize that many neuroscientists disagree, especially those who study
rodents. We respect rodents, but our ancestors diverged from theirs long ago, and primate
brains have changed immensely in the meantime. Rodent brains have changed, too.
In addition, some readers might find our neglect of comparative psychology surpris-
ing. These studies place the impressive cognitive capacities of our fellow animals beyond
doubt, but without generating the kinds of comparisons we need to understand the evo-
lution of memory systems. Instead of comparing the psychology of modern animals, we
attempt to understand the adaptations of various ancestors in their time and place.
Likewise, we do not discuss genetic, cellular, or molecular mechanisms. We take it for
granted that the central nervous system stores information by adjusting synaptic weights
in distributed neural networks. Gene expression, post- translational processing, and
protein metabolism— in both presynaptic and postsynaptic components of the relevant
neurons— lead to memory formation. If wrong, it hardly matters for our purposes. This
book deals with memory at the level of anatomically defined brain systems.
Terminology
Our discussions avoid formal taxonomy, such as Sus scrofa for pigs. There is a place for
that, but this is not that place. For our purposes, common names will do. We also resort
to convenient but slightly erroneous group names from time to time. When we discuss
monkeys without further specification, we mean macaques. Other monkeys may com-
plain if they like, but most primate research involves these species. Likewise, we rarely dis-
tinguish among the various species of macaques, although we know that they do so with
alacrity. By animals and primates, we usually exclude people but sometimes include them,
as seems appropriate to the context. Primates are “us” sometimes, at other times “them.”
When we use a phrase like “monkey neuropsychologist,” we trust readers to realize that it
refers to research on monkeys and not to simian scientists. This is not Planet of the Apes.
* Throughout the book, references and links to other sections look like this. If no chapter is specified, then
the reference is to a section heading within a given chapter.
Acknowledgements
We thank Martin Baum, Charlotte Greene, and Matthias Butler, our editors at Oxford
University Press, for their many efforts on behalf of this book. We also thank colleagues
who provided comments on selected chapters: Donna Addis, Matthew Apps, Morgan
Barense, Mark Baxter, Philip Browning, Tim Bussey, Steve Chang, Paul Cisek, Audrey
Duarte, Melissa Duff, Jon Kaas, Leah Krubitzer, Matthew Lambon Ralph, Mark Laubach,
Andrew Lawrence, Daeyeol Lee, Lynn Nadel, Dick Passingham, Karalyn Patterson,
Charan Ranganath, Peter Rudebeck, Matthew Rushworth, Lisa Saksida, Reza Shadmehr,
Matthew Shapiro, Georg Striedter, and Charlie Wilson. Conor Bloomer provided invalu-
able help with the page proofs. We also express our gratitude to Andrew, Jamie, and
Benedict Lawrence. Without their support of this endeavor, one of the authors, and by
default the others, might never have finished the book. We also thank Reza Shadmehr for
providing the anecdote that begins Chapter 6.