Table Of ContentMemory From
A to Z: Keywords,
Concepts, and Beyond
Yadin Dudai
OXFORD UNIVERSITY PRESS
01_Pre.qxd 9/9/02 9:25 AM Page i
Memory
From A to Z
Keywords, Concepts, and Beyond
Yadin Dudai
The Weizmann Institute ofScience,Rehovot,Israel
1
1
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Preface
This book contains terms that I wish my students to Howard Eichenbaum, Mark Konishi, Serge Laroche,
know.I hope that the book will also be ofinterest to Joseph LeDoux,Rafi Malach,Henry Markram,Randolf
additional audiences.Over the years,the members of Menzel, Richard Morris, Karim Nader, Lars Nyberg,
my research group have joined in from a variety of Noa Ofen-Noy,Robert Rescorla,Nava Rubin,Dov Sagi,
backgrounds,ranging from psychology via biology to Menahem Segal,Roni Seger,Alcino Silva,Burton Slot-
computer science. The common denominator was nick,Wendy Suzuki,and Misha Tsodyks.I am grateful
always keen interest in the marvels of *memory.1To to them all for their wise advice,although,of course,
facilitate the translation of this interest into science, they should be blamed for nothing.
the members ofthe team must master a language.This I am particularly grateful to my wife,Rina,for her
is an attempt to present and explain selected elements loving support,keen interest,and shrewd comments.
in this language.The fact that the science ofmemory I also appreciate the reactions of many students
is but one branch of science, combined with the who attended my lectures at the Weizmann Institute
unavoidable idiosyncrasy in the selection,resulted in of Science, the University of Edinburgh, New York
the inclusion in the book of some terms that are University, and the Gulbenkian Institute of Science,
shared by other sectors of the scientific *culture Oeiras,Portugal.Major parts ofthis book were written
as well. at the Weizmann Institute,and others at the Center for
The entries can be read as is.They may also be used Neuroscience, University of Edinburgh, and at the
as a versatile tool kit:a source for definitions,informa- Center for Neural Science,New York University.I am
tion,and further reading;a trigger for contemplation grateful to Joe LeDoux and Richard Morris for their
and discussion; and an aid to study, teaching, and friendship and for being such patient and kind hosts.
debates in classes and seminars.The entries are not a Thanks go also to Tom Boyd from the Royal Society,
replacement for comprehensive professional reviews; London, for the reference on the first use of the
they could,however,incite interest in further delving *mouse in scientific experiments;to Francis Colpaert
into the literature. In writing the entries, I tried to for advice on the *state-dependent learning literature
follow the advice ofPoe (1846) that the optimal length and for Collin’s The moonstone (1868/1992); to Liba
ofan item should fit to be read in a single sitting.I do Cehrnobrov and Anna Llionsky from the Wix Central
realize that cutural respect for the exploitation of Library services at the Weizmann Institute,to Shoshi
human *attention span has probably declined over the Hazvi from the Department of Neurobiology at the
past 150 years,but still,I hope that I did not deviate Weizmann Institute,and to librarians at the University
much from Poe’s *criterion. ofEdinburgh and New York University,for assisting me
The definition(s) at the beginning ofeach entry,and in obtaining hard-to-get copies ofenjoyable books and
the ones scattered throughout the text introduce into articles.Reading these sources reinforced my convic-
this book elements of a lexicon. The humble fate of tion that some important questions, ideas, and even
lexicographers did not escape my notice: ‘…these answers are much older than we tend to pretend,a fact
unhappy mortals… can only hope to escape reproach, oflife that should be occasionally *recalled and re*con-
and even this negative recompense has been granted to solidated in our *collective memory.
very few’(Johnson 1755).A number ofcolleagues have
read versions ofselected entries and provided the right
combination ofencouragement and reproach.Among
them were Ehud Ahissar,Amos Arieli,Diego Berman,
Aline Desmedt,Haim Garty,Patricia Goldman-Rakic,
1Throughout the text,terms preceded by an asterisk refer to entries
in the book.
iii
Acknowledgements
Permission granted by authors and publishers to adapt London; Fig. 31, Elsevier Science; Fig. 32, American
material for the preparation of figures is gratefully Psychological Association; Fig. 33, Academic Press;
acknowledged;the particular sources are accredited in Fig. 34, Cambridge University Press; Fig. 35, Oxford
the appropriate figure legends. Material copyrighted University Press;Fig.36,Cambridge University Press;
by the following publishers was used with permission Fig.38,Yale University Library;Fig.40,Elsevier Science;
in preparation ofthe following figures:Fig.1,Oxford Fig. 44, Elsevier Science; Fig. 45, Elsevier Science;
University Press; Fig. 2, Society for Neuroscience, Fig. 47, Nature Publishing Group, London; Fig. 50,
Washington,DC;Fig.3,Oxford University Press;Fig.6, Oxford University Press;Fig.51,University ofNebraska
Wiley-Liss, a subsidiary of John Wiley & Sons, Inc.; Press; Fig. 54, American Psychological Association;
Fig.7,Springer-Verlag;Fig.8,Pearson Education,UK; Fig.56,Elsevier Science;Fig.60,Taylor & Francis,UK
Fig.9,National Academy ofScience,Washington,DC; and The Psychonomic Society,Austin,TX;Fig.61,The
Fig. 10, Kluwer Academic/Plenum Publishers and Guildford Press,NY;Fig.64,Clarendon Press,Oxford;
MIT Press; Fig. 11, Oxford University Press and The Fig.65,The Psychonomic Society,Austin,TX.
American Physiological Society; Fig. 18,Nature Pub- Cover: Insets (from left to right): Augustine, as
lishing Group, London; Fig. 20, British Psychological depicted by Botticeli (Uffizi Gallery,Florence;*classic);
Society and Cambridge University Press; Fig. 22, Learning-dependent changes in the activity ofhuman
Elsevier Science; Fig. 23, Nature Publishing Group, cortex,as detected by fMRI (*functional neuroimaging,
London;Fig.24,Carl Donner,Scientific American Inc., *skill;courtesy ofAvi Karni);Neurons in the *cerebral
NY and Oxford University Press; Fig. 26, Cambridge cortex (courtesy ofHenry Markram).
University Press; Fig. 27, Nature Publishing Group,
iv
Contents
The conceptual framework 1 Dimension 82
A priori 3 Dopamine 84
Acetylcholine 4 Drosophila melanogaster 85
Acquisition 6 Engram 87
Algorithm 8 Enigma 89
Amnesia 10 Episodic memory 91
Amygdala 12 Experimental extinction 94
Anthropomorphism 14 False memory 95
Aplysia 15 Fear conditioning 97
Artefact 17 Flashbulb memory 99
Assay 19 Forgetting 100
Associative learning 20 Functional neuroimaging 102
Attention 22 Generalization 106
Behaviourism 24 Glutamate 108
Bias 25 Habit 110
Binding 26 Habituation 112
Birdsong 28 Hippocampus 114
Calcium 30 Homeostasis 117
Capacity 31 Homo sapiens sapiens 119
Cell assembly 33 Homunculus 121
Cerebellum 34 Honeybee 122
Cerebral cortex 38 Immediate early genes 124
Classic 41 Imprinting 125
Classical conditioning 44 Infantile amnesia 127
Clever Hans 47 Insight 128
Coincidence detector 49 Instrumental conditioning 130
Collective memory 51 Internal representation 133
Conditioned taste aversion 52 Intracellular signal transduction cascade 135
Confabulation 54 Ion channel 137
Conscious awareness 57 Late response genes 139
Consolidation 59 Learning 140
Context 61 Learning set 143
Controls 63 Level 145
CREB 65 Limbic system 146
Criterion 68 Long-term potentiation 148
Cue 69 Lotus 151
Culture 71 Map 152
Declarative memory 73 Maze 155
Delay task 75 Memory 157
Dementia 77 Metamemory 158
Development 79 Metaphor 160
v
Contents
Metaplasticity 161 Rat 208
Method 163 Real-life memory 209
Mnemonics 165 Recall 210
Model 168 Receptor 212
Monkey 169 Recognition 214
Mouse 171 Red herring 216
Neurogenetics 172 Reduction 217
Neurotransmitter 174 Reinforcer 219
Nootropics 176 Retrieval 221
Noradrenaline 178 Scoopophobia 224
Nutrients 179 Sensitization 225
Observational learning 180 Simple system 227
Ockham’s razor 182 Skill 229
Palimpsest 184 Spaced training 232
Paradigm 185 State-dependent learning 233
Percept 187 Stimulus 234
Performance 189 Subject 237
Persistence 190 Surprise 238
Phase 192 Synapse 240
Phrenology 194 System 242
Planning 196 Taxonomy 244
Plasticity 198 Transfer 247
Priming 200 Working memory 249
Prospective memory 202 Zeitgeist 251
Protein kinase 203 References 253
Protein synthesis 206 Subject index 321
vi
The conceptual framework
The premises that underlie the selection of Each entry opens with a definition,or a set ofdefini-
entries, the adaptation and formulation of tions. What a definition is, is extremely difficult to
definitions,and the views expressed in this book. define.A liberal list contains no less than 18 different
species of definitions, and multiple candidate defini-
I am a functionalist1with a biologist’s *bias and with tions of the definitions in each species (Robinson
*conscious awareness ofother disciplines.My approach 1954).Whenever possible,I tried to adhere to one of
to memory research is guided by the following tenets: the following meanings ofdefinition:(a) the minimal
(a) the function of the brain is to create and retain set of attributes that uniquely describes an item or a
*internal representations ofthe world that could guide concept;and (b) the formulation of a thing in terms
behaviour;(b) the function of*learning is to permit the of a more elementary level of organization or theory.
adaptation of internal representations to a changing These meanings are not mutually exclusive,and reflect,
world (*memory is the retention ofthese adaptations respectively,an attempt to adhere to *Ockham’s razor,
over time); (c) learning and memory require neural and the basic reductionistic approach,which has been
*plasticity for their actualization;and (d) learning and restrained above.It is evident,however,at the outset,
memory are *system properties,made possible by the that each ofthese types ofdefinitions requires quite a
concerted operation ofmultiple *levels ofthe system. lot of*a priori knowledge about the item to be defined.2
The aforementioned tenets yield two important In the case ofmany items and concepts in the field of
consequences for memory research.First,the compre- memory research, the relevant knowledge is yet
hensive investigation ofthe processes and mechanisms unavailable.I had,therefore,to use an additional type
ofbiological learning and memory requires a multilevel ofdefinition:explanation ofthe meaning ofthe term as
approach. Second, in the analysis of learning and it is to be used (stipulated definition).And as terms in
memory,two levels offunctional organization are par- memory research are occasionally used in more than
ticularly critical.One is the behavioural level.It does one way,I provided multiple definitions when appro-
not make sense to address the function of the system priate. The difficulties and uncertainties involved in
without addressing its input–output relationships. definitions bring to mind the view that attempts to
The other is the level in which the specific content define entities at the cutting edge ofknowledge could
(semantics) ofinternal representations emerges in the cause more harm than good:‘For when we define,we
brain. Identification of the behavioural level is self- seem in danger of circumscribing nature within the
evident.Identification ofthe level that encodes internal bounds of our own notions’ (Burke 1757). There is,
representations is not. It is currently believed that however, the opposite view, that the risk is well
the level critical for encoding the semantics ofinternal worth taking.Socrates leads Meno to admit that defini-
representations in the brain is the circuit level,or the tions are always a must for a fertile,constructive dia-
cellular-and-circuit level. More reduced levels imple- logue (Plato,Meno79d;*culture).In this debate,while
ment plasticity, but in the absence of the circuit being aware ofBurke’s caveat,I am much in favour of
*context, do not suffice to endow the representation Meno’s conviction.
with its semantics.It is essential,therefore,that research Each entry ends with a short string of *associa-
programmes on memory never lose sight ofthe circuit tions. Bodies of knowledge in general are associative
and the behavioural levels.This is not easy.The circuit systems. I tried to *reinforce this notion by propos-
level is often excessively complex, the behavioural ing selected associations.The reader is invited to form
level amazingly tricky. Furthermore, the remarkable additional ones. Associations are not only aids to
success of molecular neurobiology is enticing. I thus understanding, they are also proven *mnemonic
believe in a focused,restrained *reductionistic approach devices:the richer the associative network,the higher
to memory research (Dudai 1992).I hope that this is the probability that the item will be stored (*metaphor)
aptly reflected in the entries throughout this book. and *retrieved.
1
The conceptual framework
way they are integrated with each other (Block 1980).Still,the struc-
1Functionalism in its broadest sense is any view that analyses some-
ture of the parts and of the integrative system matters solely as much
thing in terms of how it functions (Lacey 1996).There are several ver-
as it implements or shapes the function.Functional analysis is the
sions of functionalism,one of which is ‘functional analysis’ (Cummins
sense of functionalism implied here.
1975).This is the research strategy that relies on the decomposition
of a *system into its component parts while attempting to explain the 2On this difficulty,which is also called ‘the problem of the criterion’,
working of the system in terms of the capacities of the parts and the see *criterion.
2
A Priori
It is the epistemological connotation of‘a priori’that
A Priori
interests us here. Furthermore, we focus on only a
limited portion of the universe:the individualorgan-
1.Independent of experience.
ism, its brain, behaviour, and memory. Construing
2.Beforehand. ‘experience’in definition 1 as any behavioural or physi-
ological experience of the individual,leaves only one
A priori it could be assumed that students and aficiona- source ofa priori knowledge in the individual brain:the
dos of memory will benefit from contemplating the genetic material.Genes carry information about a vari-
concept of ‘a priori’. Before defending the aforesaid ety ofbehavioural capabilities and capacities (*neuro-
statement,however,a briefclarification ofthe different genetics).This information is hence ‘innate’.1As far as
meanings and uses of‘a priori’is appropriate. the individual is concerned,this is bona fide a-priori
Prior to the eighteenth century,the pair ofterms ‘a knowledge.For the species it is not,because the knowl-
priori’/‘a posteriori’(Latin for ‘from what is earlier’/‘for edge is supposed to have been acquired over time, a
what comes after’) was used to distinguish between posteriori,by natural selection in evolution.However,it
modes ofreasoning:‘The mind can discover and under- is also useful to consider as ‘a priori’that knowledge
stand the truth… by demonstration.When the mind that cannot be explained solelyby the individual’s expe-
reasons from causes to effects, the demonstration is rience.Such knowledge is generated by *developmental
called a priori;when from effects to causes,the demon- processes,via the interaction ofgenes and environment
stration is called a posteriori’ (Arnauld 1662). Only in prenatal and early postnatal periods. It is also
later were these nonidentical terminological-twins used produced throughout life by the endogenous activity of
to refer to types ofknowledge:knowledge independent the brain, which depends on the processing of both
of experience is ‘a priori’, that which is grounded in innate and acquired knowledge.Definition 2 is collo-
experience is ‘a posteriori’(Kant 1781). Traditionally quial:according to it,‘experience’is ‘experience at the
since then,the pair ‘a priori’/‘a posteriori’is associated present time’, e.g. while on a learning task. Hence
in the philosophical discourse with two other pairs of according to this liberal interpretation any experience
opposites: ‘analytic’ vs.‘synthetic’, and ‘necessary’ vs. provides a priori knowledge for future experiences.
‘contingent’(Moser 1987;Grayling 1997).A statement This connotation ofa priori gravitates toward the triv-
is ‘analytic’ if its truth value can be determined by ial,and will not be further discussed here.
understanding the concepts or terms contained in it, A priori knowledge of both innate and postnatal
whereas it is ‘synthetic’ifin order to determine its truth origin fulfils multiple roles in behaviour and behav-
value we must know how the concepts or terms ioural*plasticity:
involved relate to other constituents of the world. 1.Innate knowledge underlies reflexes and predeter-
Hence,adapting a commonly used illustration,‘singles mined behavioural routines such as used in feeding,
are unmarried’is analytic,because ‘single’is ‘unmar- mating, fighting, and fleeing (Lorenz 1981; Dudai
ried’,whereas ‘singles are happy’is synthetic,because it 1989).These behaviours vary in their dependency on
is not evident from ‘singles’how their mood should be postnatal experience.Some are essentially independent
(the latter statement also demonstrates that some kinds of experience,although they still may be perfected or
of truth are *context specific or in the eye of the modified by it,e.g.α-type *classical conditioning.Other
beholder,but this is another story).In formal terms,an behaviours require experience for maturation, fine
analytic statement is thus a tautology, and its truth tuning, and optimal *performance. This experience
value follows necessarily.The latter property leads us may have to be provided during a restricted ‘sensitive
to the third related pair of opposites: ‘necessary’ vs. period’ in life, as in *imprinting (Lorenz 1981) and
‘contingent’.‘Necessary’refers to statements that must *birdsong (Nelson and Marler 1994). Another, more
be either true or false due to what they state,whereas in general type of‘prepared’or ‘constrained learning’,in
‘contingent’ statements the truth value is contingent which the type of associations, but not their actual
upon other occurrences or relationships in the world. content,is constrained a priori,is *conditioned taste
Discussion ofthe ‘necessary’/‘contingent’pair is within aversion:we are inclined a priori to associate the taste
the realm ofmetaphysics,the ‘analytic’/‘synthetic’pair of foodstuff with subsequent visceral malaise but not
deprives logicians of sound sleep, whereas ‘a priori’/ with a painful blow to the skin (Garcia et al. 1968).
‘a posteriori’ is within the domain of epistemology Admittedly,most philosophers would not like the use of
(the science ofknowledge) (Moser 1987;Grayling 1997; the term ‘knowledge’ in the context of such ‘simple’
Bealer 1999). behaviours:‘No philosopher will be disturbed ifLorenz
3
