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Introduction
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Olfaction, Emotion and the Amygdala: Hughes
Proust Phenomena
The ability of odours to spontaneously cue
highly vivid, affectively toned, and often very
old autobiographical memories is known as
the Proust phenomenon (Chu & Downes,
2000) and is derived from the experiences of
Proust himself (1922):
And soon, mechanically, weary after a dull
day with the prospect of a depressing morrow,
I raised to my lips a spoonful of tea in which I
had soaked a morsel of cake. No sooner had
the warm liquid, and the crumbs with it,
touched my palate than a shudder ran through
my whole body, and I stopped, intent upon the
extraordinary changes that were taking
placeI was conscious that it was connected
with the taste of tea and cake, but that it
infinitely transcended those savours, could
not, indeed, be of the same nature as theirs.
Such experiences are not limited to the realm
of artistic license. A survey by the National
Geographic (Gilbert & Wysocki, 1987) gave
readers a set of six odours on scratch-and-sniff
cards. From a sample of 26 200 (taken
randomly from >1.5 million responses), ~55%
of respondents in their 20s reported at least
one emotional memory cued by one of the six
odours.
Figure 1 Simplified schematic illustrating neuroanatomical and systems-level interactions during the generation of odourevoked emotional memories.
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Olfaction, Emotion and the Amygdala: Hughes
Examination of true
autobiographical memories
Owing to problems of quantitative
measurement and application of close
experimental controls, only a limited number
of studies exist which have directly examined
Proustian phenomena.
Laird (1935) wrote about a survey of odours
as revivers of memories and provokers of
thoughts in 254 living men and women of
eminence. More than four out of five of those
surveyed reported olfactory-cued memory
experiences that were described as vivid,
emotional and old. 76% of women and 46% of
men reported that odour-cued memories were
amongst their most vivid with only 7% of
women and 14% of men describing these
memories as hedonically neutral.
Contemporary studies employ more scientific
and empirical approaches, for example the
single-cue comparison method. Data is
collected on memories that are retrieved in
response to odours and are directly compared
with those retrieved in response to stimuli
from other sensory modalities. Rubin et al.,
(1984) found that odour-cued memories were
thought of and spoken of with less frequency
than those cued by other stimuli. Contrary to
Proustian expectations, no differences were
found between different cue types, and
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
COApl
TR
PAA
COAa
PA
BLAp
BMAp
BMAa
Medial prefrontal,
agranular insular
perirhinal,
hippocampal cortex
FS
ACB
CEA
MEA
SI
THpg
PB
Figure 2 Major neural inputs and outputs of the main olfactory system as they relate to the rat amygdala (adapted from
Swanson and Petrovich, 1998). Abbreviations: ACB, nucleus accumbens; BLAp, basolateral nucleus amygdala, posterior
part; BMAa,p, basomedial nucleus amygdala, anterior, posterior parts; CEA, central nucleus amygdala; COAa,pl, cortical
nucleus amygdala, anterior part, posterior part, lateral zone; d, medial hypothalamic defensive behavior system; FS, fundus
of the striatum; i, medial hypothalamic ingestive behaviour system; LHAcl, lateral hypothalamic area, caudolateral part;
MDm, mediodorsal nucleus thalamus, medial part; MEA, medial nucleus amygdala; PA, posterior nucleus amygdala; PAA,
piriform-amygdala area; r, medial hypothalamic reproductive behavior system; SI, substantia innominata; THpg, thalamus,
perigeniculate region (includes medial geniculate complex, posterior limiting nucleus, and parvicellular subparafascicular
nucleus); TR, postpiriform transition area.
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
NTS
GABA
GR
cAMP
NA
OP
Opioid agonists and
antagonists
Projections to
STRIA
other brain
TERMINALIS?
structures
GR
BASOLATERAL AMYGDALA
vagus
nerve
BLOOD-BRAIN BARRIER
Corticosterone
Figure 4 Schematic summarizing the interactions of neuromodulatory influences in the basolateral amygdala on
memory storage. Abbreviations: 1 = 1-adrenoceptor; 1 = 1-adrenoceptor; cAMP = cyclic 35 adenosine
monophosphate; GR = glucocorticoid receptor; NA = noradrenaline; NTS = nucleus of the solitary tract; OP =
opioids (adapted from McGaugh et al., 2000).
2000).
Amygdala
mediation
of
neuromodulatory influences on
memory storage
Noradrenaline (NA) release in the brain may
regulate memory consolidation (Kety, 1972).
Gold and van Buskirks finding (1978) that
adrenaline and footshock induce the release of
NA in the forebrain of rats has provided
evidence consistent with Gerard and Ketys
suggestions. Contemporary studies now
indicate that NA release within the amygdala
is critically important in enabling
neuromodulatory influences on memory
storage. Post-training intra-amygdala infusions
of -adrenoceptor antagonist propranolol
block adrenaline effects on memory storage
(Liang et al., 1986) and post-training infusions
of NA or the -adrenoceptor agonist
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
Figure 5 (A) Amygdala activity while watching a series of emotionally arousing films correlated very highly with longterm (three-week) recall of the films. (B) Amygdala activity in the same subjects while viewing a series of relatively
emotionally neutral films did not correlate significantly with recall (reproduced with kind permission from Cahill et al.,
1996, 1996 by PNAS).
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Olfaction, Emotion and the Amygdala: Hughes
Figure 6 Functional anatomy of temporal activations during affect-laden autobiographical memory, as indicated by PETmeasured changes in rCBF. This figure details the functional anatomy of temporal activations associated with
autobiographical memory and their relationship to underlying anatomy. N.B. Activations are predominantly on the right
(left image corresponds to subjects left) and include temporomedial, temporolateral, and insular cortices. Red-cross hair
indicates local maximum within area of activation (reproduced with kind permission from Fink et al., 1996, 1996 by the
Society for Neuroscience).
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
Discussion
In this section I propose a unification between
various neural mechanisms, outlining some of
the processes that may be involved in
encoding and retrieval of emotionally toned
odour-evoked memories. Figures eight and
nine aim to bring together a portion of the
large and diverse body of evidence related to
olfaction, emotion, and the amygdala.
So why do odours act so effectively as cues for
certain emotionally toned, vivid, and old
autobiographical memories? At encoding, the
subject is emotionally aroused due to the
context, resulting in systemic release of
adrenaline and corticosterone. Noradrenergic
activation of the BLA results in the
situation/memory being labelled as a priority
for LTM storage. Hence, the episode is
preferentially encoded in brain areas via the
stria terminalis. However, this arrangement
alone does not suffice as an explanatory
concept as to why odours are better than other
sensory modalities at evoking those memories
that are particularly emotionally toned.
Here, I think that it must be related to the
direct input of olfactory stimuli into the
amygdala. There is a connection from the main
olfactory bulb to the post piriform area to the
BLA. Do olfactory stimuli (present at the time
of arousal) therefore have the opportunity to
become better associated with these emotional
memories than stimuli from other sensory
modalities (which must first travel through a
series of cortical association areas before
eventually reaching the amygdala)? The end
result of this encoding process is the formation
of a memory trace with very strong olfactory
associations. This is in agreement with the
differential encoding bias hypothesis
whereby cues do not differ in terms of their
efficacy in retrieving event details, but in
terms of the types of event with which they
become associated and consolidated in
memory.
At retrieval, the presence of the same odour as
that present at encoding cues the recall of the
original episode. As this memory is so
emotionally toned, sympathetic activation
occurs and there is concomitant retrieval of
memory and emotion. Recall is centred on
Clinical applications
Several clinical disorders involve olfactory
impairments and/or pathology in structures
associated with higher level olfactory
processing. For instance, the olfactory system
shares a common neural substrate with many
of the cognitive and emotion processes that are
abnormal in schizophrenia. Schizophrenic
patients exhibit abnormalities in certain
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Olfaction, Emotion and the Amygdala: Hughes
Peripheral neural
mechanisms of
olfaction
OE
Odorant
ENCODING
MOB
Cranial Nerve I
To main olfactory
system component of
amygdala
Peripheral release
of adrenaline and
corticosterone via
HPA axis
COApl
TR
PA
BLAp
PAA
COAa
BMAp
BMAa
Adrenaline
Corticosterone
FS
ACB
CEA
MEA
BBB
MDm
Olfactory data
inputs become
more strongly
associated with
the episode
during encoding
Projections
to other
brain
structures
VAGUS
NERVE
PB
Olfactory data
inputs from the
MOB via the TR
Stria
terminalis
THpg
Enlargement
BLA
_
cAMP
NA
GR
GR
NTS
_1
Figure 8 Novel schematic illustrating some key components of the encoding process employed during the generation of
Proustian memories. See discussion for details. Abbreviations: 1, 1-adrenoceptor; ACB, nucleus accumbens; , adrenoceptor; BBB, blood brain barrier; BLAp, basolateral nucleus of amygdala- posterior part; BMAa,p, basomedial
nucleus of amygdala anterior, posterior parts; CEA, central nucleus of amygdala; COAa,pl, cortical nucleus of amygdala
anterior, posterior lateral parts; d, medial hypothalamic defensive system; FS, fundus of striatum; GR, glucosorticoid
receptor; LHAcl, lateral hypothalamic area caudolateral part; MDm, mediodorsal nucleus thalamus; MOB, main olfactory
bulb; MEA, medial nucleus of amygdala; NA, noradrenaline; NTS, nucleus of the solitary tract; OE, olfactory epithelium;
PA, posterior nucleus amygdala; PAA, piriform-amygala area; PB, parabrachial nucleus; r, medial hypothalamic
reproductive behaviour system; THpg, thalamus perigeniculate region; TR, postpiriform transition area.
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Olfaction, Emotion and the Amygdala: Hughes
Peripheral neural
mechanisms of
olfaction
Odorant
OE
RETRIEVAL
MOB
Amygdala
Overlapping regions
Retrieval of autobiographical
memory is dependent on a
restricted key network of
predominantly
right
hemispheric
temporal
cortical areas. Surrounding
satellite regions contribute
selectively
to
other
dimensions of the memory
retrieval.
Insula
Prefrontal
cortex
Brain regions
involved in
affectively toned
autobiographical
memory ecphory
Posterior
cingulate
Temporal
cortical
areas
Hippocampusparahippocampus
Recall of emotionally
charged autobiographical
memory
All structures
are right
hemispheric
Concomitant
re-experience
of emotion
Figure 9 Schematic illustrating some key components of the retrieval process employed during the recall of Proustian
memories. See discussion for further details.
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Olfaction, Emotion and the Amygdala: Hughes
Conclusion
Odours are capable of evoking very emotional
memories because of the way that such
memories are encoded originally. Due to a
spatial and temporal coincidence in the BLA,
olfactory information has the capacity to
become more strongly associated with
emotional episodes. Consequently, only odour
stimuli have the capacity to retrieve them.
Returning to Proust, some important points
need to be clarified. When an odour evokes a
Proustian (emotionally charged) memory this
involves recollection with concomitant reexperience of the emotional side of the
memory. It is not the case that the odour itself
is evoking an emotion; instead it evokes a
memory with a strong emotional component.
Similarly, at encoding, enhanced LTM storage
most probably occurs principally as a result of
emotional arousal unrelated to any hedonic
dimensions attributable to the odour present at
the time. However, the presence of an odour
that is itself emotionally arousing would
evidently contribute.
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
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Olfaction, Emotion and the Amygdala: Hughes
Acknowledgements
I thank G Arbuthnott, K Campbell, N
McLeod, and E Wood for comments and
Chlo_.
Corresponding Author
Mark Hughes
University of Edinburgh
s0090963@sms.ed.ac.uk
Centre for Neuroscience Research
Appleton Tower Level 7
George Square
Edinburgh
EH8 9LE
UK