Memory

for Odors
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 Memory
for Odors

Frank R. Schab

Robert G. Crowder

V D Psychology Press
A Taylor & Francis Group

NEW YORK A N D L O N D O N
First Published 1995 by
Lawrence Erlbaum Associates, Inc.

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Library of Congress Cataloging-in-Publication Data

Memory for odors I edited by Frank R. Schab, Robert G. Crowder,

p. cm.
Includes bibliographical references and index.
1. Smell. 2. Memory. 3. Odors. I. Schab, Frank R.
II. Crowder, Robert G.
QP458.M45 1995
152.T66—dc20 95-15183
CIP

ISBN 13: 978-0-805-80728-8 (hbk)

Publisher’s Note
 Contents

Preface vii

Chapter 1 Introduction 1
Robert G. Crowder and Frank R. Schab

Chapter 2 Odor Recognition Memory 9

Frank R. Schab and Robert G. Crowder

Chapter 3 Odor Identification 21

Rene A. de Wijk, Frank R. Schab,
and William S. Cain

Chapter 4 The Neuropsychology of Odor Memory 39

Robert G. Mair, Loredana M. Harris,
and David L. Flint

Chapter 5 Implicit Measures of Odor Memory 71

Frank R. Schab and Robert G. Crowder

v
Vi CONTENTS

Chapter 6 Imagery for Odors 93

Robert G. Crowder and Frank R. Schab

Chapter 7 Age-Associated Differencesin Memory for Odors 109

Claire Murphy

Chapter 8 Odor Memory in Nonhumans 133

Stephen F. Davis and H. Wayne Ludvigson

Chapter 9 Commentary and Envoi 159

Rachel S. H en and Eric Eich

Author Index 177

Subject Index 185

 Preface

Beginning at least with the start of modern work on cognition, the

question of how sensory experience relates to memory has been central,
as shown in the imagery argument in the 1970s and in the pervasive
issue of coding starting in the 1960s. Examining memory within a
different and, for most of us, unfamiliar modality such as olfaction
brings these questions to foreground status even more than they have
been in the past, for all sensory modalities give rise to some type of
experience and also to some type of memory. How are these related?
Here, we appreciate that knowledge and memory are both representa­
tions in the mind (brain) that were not previously available there.
Indeed, the olfactory knowledge possessed by individuals such as chefs,
wine-tasters, and Japanese Incense Masters is a wondrous kind of
expertise to the rest of us. However, our concerns here, with some
exceptions, are more with olfactory memory than with olfactory knowl­
edge, the field of memory being concerned with cases where the
temporal and spatial context in which an experience occurred are
defining attributes of it.
We were led to this project initially by conversations with our
colleague William Cain, whose agenda had for some time been to
convince workers already committed to olfaction that genuinely cogni­
tive factors indeed had an important influence on performance. We soon

vii
viii PREFACE

realized that we had been approaching the same domain with the
diametrically opposite m andate-to convince cognitive psychologists
that there was something genuinely olfactory to be considered in this
literature on memory for odor, rather than just another level of process­
ing. The research covered in these chapters should leave little doubt as
to either of these complementary propositions.
This is the first book-length project gathering information on olfaction
and memory that we know of. We have organized the field into
subfields as we see it reflected now in the first wave of scientific activity
on this subject. But we hope this will be a provocation: We hope that
questions raised here will define directions for future research, direc­
tions we cannot now anticipate. Quite specifically, we shall be delighted
if these future directions sharpen thinking about the general relation­
ship between memory and sensation as well as about remembering
odors.
Frank R. Schab
Robert G. Crowder
 1
Introduction

Robert G. Crowder
Yale University

Frank R. Schab
Opinion Research Corporation

The power of odors to unlock human memory is celebrated in literature

and anecdote but poorly documented by science. Odors, perhaps more
than other stimuli, are widely believed to evoke vivid and complex past
experiences easily: The most famous anecdotal report of an odor serving
as a powerful memory cue is, of course, Marcel Proust's recollection of
his aunt's home in the country following the smell of a madelaine soaked
in tea. Yet in contrast to the frequency with which odors are thought to
evoke memories of the past, scientific evidence is thus far scanty.
For years, voluminous data have been collected on odor sensitivity
(e.g., Amoore, 1977, 1980; Fazzalari, 1978; Jones, 1957; Van Gemert &
Nettenbreijes, 1977), whereas relatively few studies exist on memory for
odors per se. Moreover, the memory data that do exist are so far only
poorly integrated with the most modern attitudes on human memory
(Schab, 1991; Schab & Cain, 1991). One major goal of this volume is to
point the way toward a better state of affairs, one in which the study of
odor memory is legitimatized as a proper specialization and is informed
by the most promising ideas in the mainstream study of memory. We
see especially three tendencies in modern memory theory that have not
yet sufficiently penetrated the odor-memory work: memory coding,
memory and knowledge, and implicit and explicit memory.

1
2 CROWDER AND SCHAB

MEMORY CODING

The flourishing of the cognitive approach to learning and memory,

unlike earlier approaches, stressed that stimuli are not themselves
learned and retained but, rather, some format of coding is engaged by
the stimulus and provides the retained information. Thus, researchers
such as Conrad (1964) demonstrated that visually presented letters are
retained in memory through the participation of a speech code. Many of
the first demonstrations of visual imagery in memory showed shared
capacity (interference) between the use of the visual system in an
ongoing task and the simultaneous retention of information in visual
form (Bower, 1972; Brooks, 1968).
These questions of coding have scarcely been raised, much less
addressed, for odors in memory. To measure memory for odors we can
give subjects a recognition test for a previously presented set of odor
substances. A correct recognition response to an odor, such as straw­
berry, must show that something has been acquired, retained, and
retrieved. But what? The odor itself?
Other codes are possible. For example, the subject might have smelled
the substance originally, identified it as such, and generated a visual
image of a strawberry, which was retained until the time of testing.
When the same odor was presented for recognition, it again was
identified, and the generated image matched the remembered image of
the presentation episode. The smell itself was in no sense recognized
but the encoded event was—through the medium of visual imagery.
Another alternative possibility is perhaps even more plausible: The
same target odor, strawberry, was presented originally, leading the
subject to identify the smell verbally (e.g., "strawberry" or "That bubble
gum in the red and blue wrapper"). At later recognition testing,
strawberry was again presented, again verbalized in the same way as
before, and a correct match was achieved, this time on the basis of a
verbal label. (We examine this possibility in more detail in the later
section on memory and knowledge.) What we need to answer, then, is:
What is it about an odor that is learned at presentation and mediates
performance on a later memory test?
A subordinate issue, forming part of coding analysis in general, is the
concept of imagery. What sets an image apart from any memory must be
that it preserves the coding format of the original experience, untrans­
formed by any process of recoding. Thus, a visual image of a U.S. flag
must carry some one-for-one isomorphism with the object originally
seen, not a verbal description of it or a meaningful association to it
(Shepard, 1978). Visual imagery is usually the term used when the
memory was derived top-down, as from an instruction to "picture a U.S.
 1. INTRODUCTION 3

flag." The term sensory memory, or afterimage, is reserved for the case
when this same visually coded information results from actually seeing
the target object. The same opposition between top-down and bottom-
up derivation of olfactory memory activity should logically be the case.
But it must be remembered that the case needs to be made, experimen­
tally, for this symmetry before we accept it.
Hebb (1968) believed that the same neural organizations (cell assem­
blies or phase sequences) were active in the two cases. Such neural
activity derived from the sensory surface in the case of afterimages and
from top-down instigation in the case of imagery. His favorite example
was the phantom-limb phenomenon where itching, for example, may be
experienced from a part of the body that was actually removed surgi­
cally. We may suppose that the same neural centers were stimulated by
the limb itself, before amputation, and of course by some other agency
after the limb in question was amputated. We focus on the question of
odor imagery in more detail elsewhere in this volume (see Schab &
Crowder, chapter 6, this volume).

MEMORY AND KNOWLEDGE

The distinction made by researchers such as Tulving (1972, 1983)

between episodic memory and generic knowledge is overwhelmingly apt in
guiding our thought about odor memory, but largely ignored. (Tulving
preferred the term semantic memory, to distinguish from episodic memory,
but we think generic knowledge better captures the opposition between
the two.) A prototypical example of episodic memory would be recall or
recognition of a particular word as a member of a previously presented
list. Generic knowledge is tested by a question such as "What is the
plural of the word mouse?" Both queries very obviously rely on
memory, but the learning context (time and place of acquisition) is
fundamental to the episodic-memory question and quite irrelevant to
the generic-knowledge question. Holiingworth (1913) was the first to be
explicit that in recall the context is given and the target is to be
produced, whereas in recognition the target is given and the context is
to be supplied (verification of context).
In odor memory experiments of either sort, recognition, rather than
recall, is the retention measure of choice because odors obviously cannot
be produced as the targets of memory retrieval. To identify or recognize
a familiar odor by its name—as banana, shoe polish, vanilla, or what­
ever—theoretically rests on generic knowledge and not on the context of
any specific learning episode. That is, recognizing these smells neces­
sarily shows memory for odor, coded by olfactory (chemical) dimen­
4 CROWDER AND SCHAB

sions. But it does not demonstrate memory for olfactory events. For
better or worse, the psychology of memory has been based on events,
whether in the Ebbinghaus (1885/1964) or Bartlett (1932) traditions.
Twenty years' worth of sporadic experimentation on short-term episodic
recognition memory for odors (see Schab & Crowder, chapter 2, this
volume) has produced quite modest knowledge beyond dismay that
such memory is relatively at variance with conventional wisdom.
The two literatures on odor recognition and odor identification exist
side-by-side, with no efforts to recognize the distinction, much less to
make comparisons. For example, how are we to measure odor memory
performance? One classic index used in the study of olfactory func­
tioning is the ease with which subjects can name familiar odors, given a
sniff, out of context (Doty, Shaman, Krefetz, & Dann, 1981; Douek,
1974). But just as odor identification decrements may reflect impaired
sensory functioning or odor discrimination or impaired odor identifica­
tion, or some combination of these, so may episodic odor memory
performance reflect both episodic and generic odor memory. The
knowledge-versus-memory issue is not all independent of the coding
question we just discussed: If episodic recognition testing of odors were,
at least partially, dependent on a verbal/semantic code, for normosmics
(people with an unimpaired sense of smell), then a deficit in generic
odor recognition would show up disguised as an episodic recognition-
memory deficit. For example, subjects could cope with an episodic
memory experiment by (a) first identifying the inspection odors with a
verbal label or semantic association ("This is strawberry" or "This smells
like that gum in the blue and red wrapper" or "This reminds me of
summer visits to Grandpa's") and then (b) remembering these verbal/
semantic associations until the recognition testing, at which point they
(c) identify the recognition candidates with the same verbal labels or
semantic associations and (d) match these against the memorized ones.
This would produce a theoretically spurious correlation between the
forms of memory involved in knowledge and episodic testing, for a
deficit in the episodic capacity (temporal-spatial marking of olfactory
experiences) would not produce a correlated penalty in odor naming.
For such reasons, we should be especially interested in memory
studies with odors that are difficult to name. Potentially, these allow
some degree of dissociation of the memory for an odor experience with
its identifiability. (However, even with strange odors never before
smelled, subjects may still employ some form of verbal, or at least
semantic, identification: "It smells kind of like . . ." or "It reminds me
of. . . .") If naming suffers, for such difficult-to-name odors, as it surely
does, without an appreciable decline in episodic recognition memory,
then we may be encouraged to believe that olfactory experiences can be
 1. INTRODUCTION 5

recognized, as such, with minimal participation of verbal mediation.

The objection might be raised that difficult-to-label odors would suffer in
memory experiments because of their obscurity, or unfamiliarity. How­
ever, we know from studies of verbal memory (Schulman, 1974) that
rare stimuli are recognized better than familiar ones, although recalled
worse. Recently, Schab, De Wijk, and Cain (1991) compared episodic
recognition of common (e.g., strawberry, oregano, and cigarette butt)
and uncommon (e.g., benzaldehyde, methylbutyrate, and linalyl ace­
tate) odors and found uncommon odors were recognized significantly
worse than common ones. This result, in part, may be due to difficulty
of generating and attaching verbal/semantic information to the un­
common odors. However, this is one area where additional experiments
are waiting to be done in order to integrate the study of odor memory
and mainstream principles of (verbal) memory. One important question
is: How much of episodic odor memory is memory for verbal/semantic
associations generated to the odors at inspection and testing?
The same ambiguity about the form of coding we have discussed in
episodic memory experiments (remembering the verbal description of
odors rather than the odors themselves) does not plague odor identifi­
cation, which tests memory for odors in the form of generic knowledge.
Because the name is itself the target of retrieval in such tests it could not
be an unwelcome mediator in that retrieval. Knowledge of what banana,
for example, smells like must therefore depend on some stable repre­
sentation of the precise chemical configuration.

IMPLICIT AND EXPLICIT MEMORY

One of the most exciting developments in the field of memory since the
1980s has been the emergence of tests of implicit memory. For example,
priming effects in word-stem completion give evidence for an earlier
presentation just as surely as do tests of recognition or recall. Priming is
the better measure of retention, too, in that amnesics can be shown to
have normal performance in priming (Graf, Squire, & Mandler, 1984),
whereas they are virtually helpless in explicit recall and recognition.
Such priming is also evident in tachistoscopic word recognition (Jacoby
& Dallas, 1981) and picture naming (Snodgrass & Feenan, 1990). If any
single new research trend has animated work in the area of memory
during the 1980s, it was probably the introduction of implicit memory
techniques. So far, we know of no published reports on odor memory
using implicit testing. Here, more than elsewhere, this volume is
intended as a call to action for investigators.
The notorious difficulty people sometimes have in retrieving the
6 CROWDER AND SCHAB

names of familiar odors, or recognizing such items from a short array of

episodically presented odors, suggests to some that, unlike many of our
experiences, odors fail to produce explicit, retrievable memory traces
(Engen, 1982). But is retention of odors likewise poor? Tests of percep­
tual recognition, identification, or threshold measurement all potentially
permit priming effects from some earlier experience with an odor as
compared to appropriate nonprimed controls.
We have evidence from our laboratory concerning priming in odor
naming, too (see Schab & Crowder, chapter 5, this volume), but that
field has otherwise been, so far, innocent of implicit testing methods.
Theoretical considerations do encourage the importance of implicit
memory measures for odors: Scholars such as Tulving (1983) consider
the techniques of implicit memory to be persuasive in both human and
animal species, whereas the phenomenon of explicit memory, or recol­
lection, is considered more uniquely human. What lower animal can,
like us, reflect on an experience and be transported to that same or
similar experience at some temporal remove? We shall not quibble about
the power of some advanced mammals to do something of the sort, but
surely the sorts of simple organisms from which we evolved were
simultaneously capable of retention and yet incapable of explicit recol­
lection. The chemical senses, including olfaction, were as prominent in
these early species as they are secondary to us in comparison with the
evolutionary later vision and audition. It would follow that the place to
look for olfactory retention should not be among the advanced evolu­
tionary triumphs of memory but rather among the more primitive
forms.

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 1. INTRODUCTION 7

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Introduction
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