How arousal modulates memory: Disentangling - NYU Psychology

13 Pages·2006·0.31 MB·English

Cognitive, Affective, & Behavioral Neuroscience
2004, 4 (3), 294-306
How arousal modulates memory: Disentangling
the effects of attention and retention
TALI SHAROT andELIZABETH A. PHELPS
New York University, New York, New York
Emotion may influence memory both by altering attention and perception during encoding and by
affecting memory retention. To date, studies have focused on the enhancement of memory consolida-
tion by arousal. However, they have failed to rule out a role for attention. To specifically link memory
enhancement of arousing material to modulation of memory retention, we examined recognition of
neutral and arousing words at two time points and under conditions that manipulate attention during
encoding. Participants were briefly presented with an arousing or neutral word at the periphery, while
fixating on a central word. Recognition of peripheral words was assessed either immediately or after
24h. Whereas recognition of neutral words became worse over time, recognition of arousing words re-
mained the same and was better than neutral word recognition at delay. The results indicate that
arousal supports slower forgetting even when the difference in attentional resources allocated to stimuli is
minimized.
Memory enhanced with emotion has been documented into the amygdala (Liang, Juler, & McGaugh, 1986), a
across a range of memory studies including field studies strong indication that the enhancement effect occurs after
(e.g., Bohannon, 1988) and laboratory studies, with stim- initial encoding.
uli such as emotionally charged stories (e.g., Heuer & Findings from human studies support the notion that
Reisberg, 1990), film clips (e.g., Cahill et al., 1996), memory is influenced by emotional arousal via amygdala
words (e.g., LaBar & Phelps, 1998), and pictures (e.g., activation and the adrenergic system. Adrenergic receptor
Bradley, Greenwald, Petry, & Lang, 1992; Christianson antagonists have been shown to block the modulation of
& Fallman, 1990). It has been suggested that emotion memory by emotional arousal in humans (Cahill, Prins,
may influence memory in two different ways, by altering Weber, & McGaugh, 1994). Neuroimaging studies have
attention and perception during encoding (Christianson reported a correlation between long-term memory of emo-
& Loftus, 1991; Reisberg & Heuer, 1992) and by affect- tionally arousing stimuli and degree of amygdala activa-
ing memory retention (Kleinsmith & Kaplan, 1963). tion during encoding (Cahill et al., 1996; Hamann, Ely,
Examination of the neural mechanisms underlying mem- Grafton, & Kilts, 1999), as well as enhanced amygdala ac-
oryof emotional events has predominantly focused on the tivation during retrieval of emotional items (Dolan, Lane,
latter, and suggests that adrenal stress hormones related to Chua, & Fletcher, 2000). Furthermore, emotional arousal
emotional arousal are crucial for allowing the significance fails to enhance long-term memory of arousing words in
of an event to enhance hippocampal-dependent memory patients with selective lesions of the amygdala (LaBar &
consolidation of that experience (McGaugh, 2000). The Phelps, 1998).
amygdala, a small almond-shaped structure in the medial However, studies conducted with humans have not been
temporal lobe adjacent to the hippocampus, is critical in able to rule out a role for attention in the enhancement of
mediating the influence of stress hormones that activate memory retention that occurs with emotional arousal. Un-
adrenergic receptors on memory strength (McGaugh, like studies conducted with nonhuman animals, which
2000). Amygdala lesions block the strengthening effects have shown an effect on later memory by postencoding
of these modulators on memory consolidation, as does arousal or pharmacological manipulation, studies with hu-
posttraining infusion of β-adrenergic receptor antagonists mans have manipulated arousal at encoding and failed to
control for an effect on attention. In two studies (Cahill &
Alkire, 2003; Cahill, Gorski, & Le, 2003), an endogenous
stress hormone was administered after encoding, and the
This study was supported by the National Institutes of Health Grant
findings revealed that this manipulation enhanced later
MH62104 to E.A.P. We thank Marisa Carrasco for her assistance in the
design of the experiment, Mauricio Delgado and Barry Cohen for help- memory only for stimuli that were already arousing by
ful comments on a previous draft of this article, Nonso Enekwechi and their own properties. Thus, modulation of attention at en-
Dani Korya for their help in data collection, and Melinda Miller, Ben coding could not be ruled out. In addition, most of these
Holmes, and Laura Thomas for programming assistance. Correspon-
studies have examined memory at only one point in time
dence should be addressed to E.A. Phelps, Department of Psychology,
and have failed to determine whether the effect of emo-
6 Washington Place, Room 863, New York University, New York, NY
10003 (e-mail: [email protected]). tion on memory is enhanced over time. Without examin-
Copyright 2004 Psychonomic Society, Inc. 294
HOW AROUSAL MODULATES MEMORY 295
ing memory at different time points, immediately after consciously recognized. Masked fear-conditioned faces,
encoding as well as after a delay, and without looking at for example, evoke skin conductance changes in partici-
memory of emotional material under conditions that con- pants, even if they later fail to report perceiving those faces
trol for attention, we are unable to specifically link mem- (e.g., Öhman et al., 1995). Brain imaging studies have
ory enhancement of arousing material to modulation of also shown that processing of arousing stimuli can occur
hippocampal-dependent memory consolidation in humans. when attention is directed to a different task (Vuilleu-
The aim of this study was to explore the interaction mier, Armony, Driver, & Dolan, 2001) and in patients with
between the two elements—attention and retention— spatial neglect (Vuilleumier & Schwartz, 2001). Chris-
that influence memory of arousing stimuli, and to exam- tianson (1992) proposed that there may be elements inher-
ine whether they are both necessary for slower forgetting ent in emotional stimuli that cause them to be processed
of such stimuli. We will begin with a review of the ef- by automatic, apparently “preattentive,’’ mechanisms, thus
fects of arousal on attention and on memory storage. facilitating responses toward such meaningful stimuli.
Ochsner (2000) has suggested that by modulating the se-
Effects of Arousal on Attention lectivity of attention, enhancing attentional dwell time, and
There are a few ways by which arousal can affect at- allowing arousing stimuli to be processed more efficiently,
tention and thereby influence encoding. The first is by the distinctiveness with which arousing stimuli are encoded
modulating the selectivity of attention. Easterbrook (1959) is strengthened, resulting in more accurate memory of that
proposed that arousal will lead to the “narrowing of at- stimuli. Although such modulations of attention and per-
tention—that is a decrease in the span of cues to whichan ception by arousal may affect long-term memory, one
organism is sensitive. When observing an emotional would also expect to see the results of this influence on
event, attention will be focused primarily on the arousing memory at short delays. Indeed, better memory for arous-
details of the stimulus, resulting in better encoding of ing stimuli, as compared with neutral stimuli, has been re-
those details and impaired encoding of less relevant de- ported both for immediate recollection (e.g., Christian-
tails. In an effort to examine eye movements as an indi- son, 1984; Christianson, Loftus, Hoffman, & Loftus, 1991;
cator of the location of overt attention, studies have indeed Loftus et al., 1987) and for long-term retention (e.g.,
shown that an emotional slide elicited eye movements con- Cahill etal., 1996; LaBar & Phelps, 1998).
sistent with attentional narrowing (Loftus, Loftus,& Messo,
1987). Such selectivity could lead to better memory for Effects of Arousal on Memory Storage
central details of an arousing event at the expense of A number of studies suggest that the effect of arousal
memory for peripheral details (Burke, Heuer, & Reis- on memory is enhanced following a delay; whereas mem-
berg, 1992; Christianson & Loftus, 1991). Adolphs, Den- ories for neutral stimuli decrease over time, memories for
burg, and Tranel (2001) reported that bilateral damage to arousing stimuli remain the same or improve over time
the amygdala resulted in inferior memory for gist of (e.g., Baddeley, 1982; Kleinsmith & Kaplan, 1963; La-
aversive scenes but better memory for visual details of Bar & Phelps, 1998; Levonian, 1966; Walker & Tarte,
those scenes, suggesting that the amygdala may play a role 1963). Research on the neural mechanisms of memory for
in filtering relevant information from stimuli that signal arousing events indicates that arousal leads to enhanced
threats during encoding. A second way by which arousal long-term memory of stimuli by altering hippocampal con-
can influence attention is by enhancing attentional dwell solidation of these memories (Cahill, Babinsky, Markow-
time on the arousing stimuli and delaying the disen- itsch, & McGaugh, 1995; Hamann etal., 1999; McGaugh,
gagement component of attention (Fox, Russo, Bowles, 1992; Packard & Teather, 1998). It has been suggested that
& Dutton, 2001). the slow consolidation of memories serves an adaptive
Arousal may also modulate attention by allowing such function by enabling neurohormonal processes triggered
stimuli to be processed more efficiently (Hansen & Han- by an arousing stimulus to modulate memory strength
sen, 1988), achieving awareness with less attentional re- (McGaugh, 2000). In a classic study, Kleinsmith and Ka-
sources. Anderson and Phelps (2001) have shown that plan (1963) found that after a 1-week delay, participants
under settings of limited attention for normal perceptual recalled significantly more numbers paired with arousing
awareness (the attentional blink), normal participants words than with nonarousing words. They also found that
showed enhanced perception of aversive arousing words the reverse was true for participants given an immediate
compared with nonarousing words. In fact, it has been test. Other studies since have shown a similar pattern of
suggested that arousing stimuli can be processed even results (e.g., Baddeley, 1982; Levonian, 1966; Walker &
when the stimuli appear outside the focus of attention and Tarte, 1963). Although the significantly higher recogni-
without conscious awareness (Christianson, 1992; Öh- tion rates of numbers paired with arousing words versus
man, Estevens, & Soares, 1995). Viewing an arousing stim- neutral words in the delay test can be explained by emo-
ulus for a very brief time evokes an automatic assessment tional memory consolidation mechanisms (McGaugh,
of it (Bargh, Chaiken, Govender, & Pratto, 1992). Height- 2000), the reason underlying the poorer recognition rates
ened physiological measures, which reflect an individual’s for numbers paired with arousing words found in theim-
emotional response, arise even when the stimulus is not mediate test is unclear.
296 SHAROT AND PHELPS
As consolidation of memory occurs over a period of dation became apparent and may have overshadowed those
time, the effects of arousal on enhanced memory con- of attention.
solidation will be apparent only following a delay. The Efforts have been made in the past to study memory of
exact duration of time in which consolidation takes place arousing stimuli per se (rather than those paired with
is uncertain. The behavioral affects may be evident as arousing stimuli) under conditions of restricted atten-
soon as 1 h after encoding (LaBar & Phelps, 1998) and tional resources, by utilizing short exposure times (Chris-
are expected to be visible at least 24 h later (e.g., Adolphs, tianson et al., 1991; Ochsner, 2000). These studies re-
Tranel, & Denburg, 2000; Gallagher & Kapp, 1981; Vaz- vealed that under such conditions, arousing stimuli are
darjanova & McGaugh, 1999). If arousal were to influ- still remembered better than neutral stimuli. However,
ence memory for emotional stimuli via strengthening hip- these studies (Christianson et al., 1991; Ochsner, 2000),
pocampal consolidation alone, one would expect to see like many others (Christianson, 1984; Christianson &
better memory for such stimuli relative to neutral stimuli Loftus, 1991; Christianson etal., 1991; Clifford & Hollins,
after a delay, but not immediately after encoding. 1981; Libkuman, Nichols-Whitehead, Griffith, & Thomas,
1999; Wessel, van der Kooy, & Merckelbach, 2000), ex-
Interaction Between the Effects of Arousal on amined memory for arousing stimuli only at one point in
Encoding and on Memory Storage time, usually immediately after encoding, and were thus
Although it seems probable that arousal influences unable to study the long-term modulation of memory by
memory both by mediating acquisition of arousing stim- arousal.
uli (Anderson & Phelps, 2001; Christianson & Loftus, It has been shown that processing of the arousing prop-
1991) and by modulating memory consolidation (Cahill erties of a stimulus can occur when attention is focused
etal., 1996; LaBar & Phelps, 1998), it is unclear how these on a different task (Vuilleumier etal., 2001), but do such
mechanisms interact and whether they are both neces- encoding conditions allow for enhanced retention? The
sary for enhanced memory of arousing stimuli. present study tests for the first time whether arousal can
From research with nonhuman animals, it is clear that support long-term memory of a stimulus even when
modulation of attention is not necessary for enhanced overt attention is not focused on the arousing to-be-re-
memory retention. Studies in rats demonstrate that post- membered stimulus. In contrast to Kleinsmith and Ka-
training systemic injection of epinephrine enhances long- plan’s (1963) study, this study examines memory for
term memory (Packard & Teather, 1998). Epinephrine is stimuli that are arousing for their own properties (i.e.,
an adrenal medullary hormone released in the blood- arousing words rather than numbers paired with arousing
stream when a person is in an aroused state and is one words). We investigate how the arousing property of a word
means by which arousal is thought to influence hippocam- influences the retention of that word, when overt attention
pal consolidation (McGaugh, 1992). The poststimulus is focused elsewhere during encoding. To date, no attempt
drug administration obviously excludes effects on acquisi- has been made to study memory of arousing stimuli pre-
tion or retrieval because the drug’s influence occurs after sented in the visual field periphery. The design of our study
training is completed, and the drug is inactive by the time allows us to examine the effects of overt attention and re-
of retrieval, hence supporting the notion that arousal can tention interval on recognition rates of arousing and neu-
influence memory by affecting consolidation. tral stimuli.
If one were to argue that attention was the primary In Experiment 1, participants were very briefly ex-
mechanism underlying the superior memory of arousing posed to a neutral word at the center of the screen and at
stimuli relative to neutral stimuli, one would expect to the same time to either an arousing or a neutral word at
see better memory for these stimuli, both immediately the periphery. To engage attention at the center, partici-
and after a delay. Given this assumption, however, one pants were asked to fixate the central word and to make a
would have a difficult time interpreting Kleinsmith and frequency judgment regarding that word. Recognition for
Kaplan’s (1963) results, showing an advantage for num- all words was assessed either immediately or after 24 h.
bers paired with arousing words over those paired with
neutral words only at delayed test, but not at immediate
EXPERIMENT1
test. In some respects, by looking at cued recall for num-
bers paired with arousing or nonarousing words, Klein-
Method
smith and Kaplan were examining memory for a neutral
Participants. The participants were 50 undergraduates at New
peripheral detail (the paired numbers) of an event. Al-
York University (29 females and 21 males, between 18 and 28 years
though participants were given enough time to study the of age). The participants were randomly assigned to either the im-
pairs, it is possible that attention was captured to a larger mediate test condition (n= 25) or the delayed test condition (n=
degree by the arousing words than by the neutral words. 25). All the participants provided informed consent and were either
The immediate result was a tradeoff for memory of the paid or received course credit for their participation.
Materials. Words were chosen from the list of words used by
numbers paired with these words: better memory for num-
LaBar and Phelps (1998). All words were 4–6 letters long, their size
bers paired with nonarousing words than for those paired on the screen was 5(cid:1)1cm, and peripheral words were centered at
with arousing words. However, at the delay test, for which 5º of visual angle, 5cm from fixation. (See the Appendixfor all
the results were reversed, the effect of enhanced consoli- words used in the study.) Since word norms are not available for
HOW AROUSAL MODULATES MEMORY 297
most of the arousing words used in this study, 15 undergraduates trials in a random order, with the trials including all central and pe-
from New York University, drawn from the same population as were ripheral words. In each trial, two words were shown on the screen,
the other participants in this study, rated all words for arousal, va- one old and one new. The participants were asked to indicate which
lence, and familiarity. Word familiarity was rated on a scale from 1 of the two words was shown in the first part/day of the experiment,
(not at all familiar) to 7 (very much familiar). No difference was by pressing “1” on the keyboard if the word shown on the left was
found in the ratings of familiarity for neutral (M= 5.7, SD= 0.62) the “old” word, or “9” if the word shown on the right was the “old”
and arousing [M= 5.5, SD= 0.39; t(48)= 1.35, p(cid:2).05] words. It word. Word pairs were matched for frequency and arousal (see the
has been argued that subjective familiarity ratings (e.g., Gerns- Appendixfor target words and matched foils).
bacher, 1984; Gilhooly & Logie, 1980) and subjective frequency Recognition of central words was found to be at ceiling both at the
ratings (Balota, Pilotti, & Cortese, 2001) serve as better reflections immediate (97%) and delay (96%) tests, suggesting that participants
of the relative frequency of exposure to a word than do objective were indeed engaged with the central task. Recognition scores of 5
frequency counts. participants who recognized fewer than 14 of the 16 (87.5%) central
Word valence was rated on a scale from 1 (positive) through 4 words correctly were not used, to control for the possibility that they
(neutral) to 7 (negative). Neutral words were rated as neutral (M= did not fixate the central words at all times, as instructed, and thus
3.4, SD= 0.42) and arousing words as negative [M= 5.6, SD= 0.88; correctly recognized a lower proportion of the central words.
t(48)= 11.05, p(cid:3).001]. Arousal was rated on a scale from 1 (not
at all arousing) to 7 (very much arousing). Neutral words had lower Results
arousal ratings (M= 1.96, SD= 0.42) than did negative words [M=
Recognition scores were subjected to an analysis of
3.62, SD= 0.49; t(48)= 12.93, p(cid:3).001].
variance with retention interval (immediate vs. delay) as
Preceding word rating, skin conductance responses (SCRs) to the
a between-subjects variable and word type (arousing vs.
words were recorded from participants in a pilot study, drawn from
the same population as were the other participants in this study, neutral) as a within-subjects variable. To control for
using the same paradigm as in this experiment. This was done to en- Type I errors in testing simple main effects, we used a
sure that the stimulus words caused physiological arousal under this familywise Bonferroni adjustment. Because each of our
paradigm. SCR is a phasic measure of eccrine sweat gland activity, factors had two levels, we used an alpha of .025 to test
a dependable autonomic indicator of sympathetic nervous system
each of our simple main effects (Keppel, 1991).
excitation (Venables & Christie, 1973). SCRs were recorded from
As is illustrated in Figure1, recognition scores for pe-
the third and fourth fingers of the participants’ nondominant hands
and scored according to conventional criteria (for details on the psy- ripheral words were characterized by a reliable inter-
chophysiological recording and analysis, see LaBar, LeDoux, Spen- action of word category (cid:1)retention interval [F(1,48)=
cer, & Phelps, 1995). The participants produced larger SCRs to the 7.66, p(cid:3).01]. The results of a within-subjects ttest in-
arousing words than to the neutral words [t(16)= 1.93, p(cid:3).05, one- dicate that after 24 h, recognition of arousing words was
tailed]. These findings, together with the arousal ratings, suggest
significantly higher than that for neutral words [t(24)=
that the arousal manipulation at encoding was effective in produc-
2.56, p(cid:3).02]. An independent sample ttest showed that
ing subjective and physiological arousal.
Design and Procedure. During encoding, the participants sat recognition for neutral words was better at immediate
57cm from a computer screen. There were 16 trials in which they test than at delayed test [t(48)= 2.34, p(cid:3).025]. All other
were asked to fixate a neutral word at the center of the screen, and comparisons were found to be not significant.
at the same time either a neutral word (8 trials) or an arousing word
(8 trials) appeared at one of the corners of the screen 5cm from the
Discussion
center, 5º from fixation. The intertrial interval was 10sec, and the
The findings of Experiment1 suggest faster forgetting
stimulus duration was 250msec. Given that it takes about 250msec
for nonarousing words than for arousing words, showing
for a target-directed saccade to be initiated when no other attention-
consuming task is presented (e.g., Carpenter, 1988; Mayfrank, a reliable word type (arousing vs. neutral) (cid:1) retention
Kimmig, & Fischer, 1987), this stimulus duration minimizes the interval interaction, like that reported by Kleinsmith and
probability of saccadic eye movements to the word in the periphery Kaplan (1963). The results are also consistent with pre-
in the present design. A pilot study revealed that shorter stimulus vious findings that arousing stimuli are recognized more
durations (e.g., 180msec, 200msec) resulted in a floor effect for word
accurately than nonarousing stimuli after a delay (e.g.,
recognition under all conditions. To engage attention at the center,
Cahill et al., 1995; Ochsner, 2000). These findings go
the participants were asked to fixate the central word and to indi-
cate how often they encountered that word in the English language beyond previous ones in demonstrating that arousal can
on a scale from 1 (rarely) to 5 (often) by striking a key (1–5) on the support memory retention of a stimulus, even when that
keyboard. stimulus is presented in the visual field periphery. Bet-
After the encoding phase, the participants in the delay condition ter recognition of arousing words over neutral words was
were told to return to the lab the following day in order to partici-
evident only at delayed test, and not at immediate test,
pate in a similar study. The participants in the immediate condition
supporting the notion that the primary mechanism under-
began the test phase approximately 3min after the end of the en-
coding phase, following instructions for the test phase. Informal de- lying this superior recognition is an effect of retention.
briefing revealed that the participants in both the delay and imme-
diate conditions did not anticipate a memory test. Although enhanced EXPERIMENT2
memory of arousing words may be apparent at a retention interval
shorter than 24h, previous studies have shown that the effects of con-
In order to engage overt attention at the center of the
solidation should be evident at least 24h after learning has taken place
screen, the participants were asked in Experiment1 to
(e.g., Gallagher & Kapp, 1981; Vazdarjanova & McGaugh, 1999).
Either immediately or after 24 h, a surprise two-forced-choice fixate a central word, which appeared briefly together
recognition test was given. The participants went through 32 test with the peripheral word, and to make a frequency judg-
298 SHAROT AND PHELPS
75
70
ct
e 68
orr 67
C 65
n
o
niti 62.5
g 60
o
c
e
R 57
% 55
50
Immediate Test 24-h Delay Test
Neutral Words Arousing Words
Figure1. Experiment 1: Recognition rates for peripheral words at immediate and delayed tests.
One word (either neutral or arousing) was presented at the periphery at the same time as a neutral
word was presented at the center of the screen. Brackets represent standard errors of the means.
ment regarding the central word. To minimize possible were indeed engaged with the central task. Recognition scores of 3
differential covert shifts of attention, which may be more participants who recognized fewer than 7 of the 8 (87.5%) central
frequent for arousing words than for neutral words, in Ex- words correctly were not used (see Method section in Experiment1,
for justification).
periment2 the participants were exposed simultaneously
to both an arousing word and a neutral word at the pe-
Results
riphery, while they were asked to fixate a neutral word at
Data analysis was the same as in Experiment 1 (see
the center. Such demanding conditions may make selec-
Results section in Experiment1).
tive shifts less likely. Furthermore, assuming that the
As in Experiment1, recognition scores were character-
neutral–peripheral and arousing–peripheral words were
ized by a reliable interaction of word category and reten-
now competing for a very limited attentional resource
tion interval [F(1,48)(cid:4)5.22, p(cid:3).05; see Figure2]. No
(they appeared simultaneously, rather than on separate
pairwise comparisons were found to be significant. The
trials, as in Experiment 1), if an attention mechanism
95% confidence interval for mean recognition rates of the
were underlying the pattern of results in Experiment1, a
arousing words in the immediate test (µ (cid:4)46.54%)
relatively larger difference between recognition rates lower
and of the neutral words at delay test (µ (cid:4)48.73%) in-
would be expected in the delayed test in Experiment 2, lower
dicate that in both these cases, recognition rates were not
compared with Experiment1, as well as higher recogni-
significantly different from chance (50%). However, 95%
tion rates for arousing words over neutral words at the
confidence interval for mean recognition rates of both
immediate test.
neutral words at immediate test (µ (cid:4) 56.2%) and
lower
arousing words at delay test (µ (cid:4)54.5%) were sig-
Method lower
nificantly above chance.
Participants. The participants were 50 undergraduates at New
York University (33 females and 17 males from 18 to 28 years of When the results of Experiment2 were compared with
age) assigned to either the immediate test condition (n= 25) or the those of Experiment1, no three-way interaction (time of
delayed test condition (n= 25). test (cid:1)type of word (cid:1)number of words in the periphery)
Materials. Materials were the same as in Experiment1 (see was found. We thus collapsed the results from Experi-
Method section in Experiment1).
ments 1 and 2. Overall collapsed recognition scores were
Design and Procedure. The method for Experiment2 was iden-
characterized by a reliable interaction of word category
tical to that of Experiment1, except that at the periphery a neutral
word andan arousing word appeared simultaneously either verti- (cid:1)retention interval [F(1,98)(cid:4)12.44, p(cid:3).01; see Fig-
cally or horizontally to one another at two of the four corners of the ure 3], as also found separately in both Experiments 1
screen, 5cm from the center, at 5°from fixation. As in Experi- and 2. To control for TypeI errors in testing simple main
ment1, a neutral word was presented at the center of the screen at effects, we used a familywise Bonferroni adjustment,
the same time. In Experiment2, the participants went through only
setting alpha to .025 to test each of our simple main ef-
8 trials, but they were exposed to a total of 16 peripheral words as
in Experiment1 (16= 8 trials(cid:1)2 peripheral words). As in Exper- fects (Keppel, 1991). A within-subjects t test indicated
iment1, recognition of central words was at ceiling (99%) for both that at delayed test, recognition rates of arousing words
the immediate and delayed tests, suggesting that the participants were significantly higher than those of neutral words
HOW AROUSAL MODULATES MEMORY 299
75
70
ct
e
orr 65
C
63
on 61
niti 60
g
o
ec 55 55.5
R
% 53
50
45
Immediate Test 24-h Delay Test
Neutral Words Arousing Words
Figure2. Experiment 2: Recognition rates for peripheral words at immediate and delayed tests.
Two words (neutral and arousing) were presented simultaneously at the periphery at the same time
as a neutral word was presented at the center of the screen. Brackets represent standard errors of
the means.
[t(48)(cid:4)2.86, p(cid:3).01]. At immediate testing, recogni- at delayed test than at immediate test, in accord with
tion rates of neutral words were marginally higher than Kleinsmith and Kaplan’s (1963) findings. Possible inhi-
those of arousing words [t(48)(cid:4)2.19, p(cid:4).033]. An in- bition or interference effects that may underly these trends
dependent sample ttest revealed that neutral words were are reviewed in the General Discussion section.
recognized better at immediate test than at delayed test
[t(48)(cid:4)2.75, p(cid:3).01]. For arousing words, there was a EXPERIMENT3
marginally significant effect for better recognition at de-
layed test than at immediate test [t(48)(cid:4)2.11, p(cid:4).045]. In Experiments1 and2, a neutral word was presented at
Overall recognition rates were lower in Experiment2 the center of the screen, where overt attention was focused.
(M(cid:4)58.1%, SD(cid:4)1.6), when the participants were ex- Thus, the participants were aroused only when the word at
posed to two stimuli in the periphery at the same time, than the periphery was arousing. In Experiment 3, we asked
in Experiment1 [M(cid:4)63.6%, SD(cid:4)1.6; F(1,98)(cid:4)5.88, whether a pattern of recognition rates similar to that found
p(cid:3).01]. in Experiments1 and2, would emerge if the participants
were to encounter an arousing word, instead of a neutral
Discussion one, at the center of the screen. As in Experiment1, at the
The somewhat low performance rates in Experiment2, periphery either a neutral word or an arousing word was
as compared with those in Experiment1, suggest that the presented. In this experiment, attention should be engaged
task in Experiment 2 was more demanding than that in to an even larger extent by the central word because arous-
Experiment 1. Nevertheless, even when one minimizes ing stimuli, once attended to, have been shown to engage
possible differential covert shifts of attention, the results attention to a greater degree than neutral stimuli, increas-
demonstrate once again a reliable word type (arousing ing attention dwell time at that location and influencing the
vs. neutral) (cid:1) retention interval interaction (see Fig- disengagement component of attention (Fox etal., 2001).
ure2), with no three-way interaction between the results
of Experiments1 and2. When the results of Experiments Method
1 and 2, were collapsed, recognition rates of arousing Participants. The participants were 50 undergraduates at New
York University (32 females and 18 males between 18 and 28 years
words at delayed test were higher than recognition rates
of age) assigned to either the immediate test condition (n= 25) or
of neutral words, as in Experiment1. Also, recognition
the delay test condition (n= 25).
rates of arousing words revealed an enhancement trend Materials. Materials were the same as in Experiments1 and2.
over time. These findings are consistent with the notion Design and Procedure. The method for Experiment3 was iden-
that arousal leads to enhanced long-term memory (Ca- tical to that of Experiment1 except that at the center of the screen an
hill etal., 1995; LaBar & Phelps, 1998; McGaugh, 1992; arousing word was presented rather than a neutral word as in Exper-
iments1 and2.
Packard & Teather, 1998). Additionally, there was a trend
As in Experiments1and2, recognition of central words was
at the immediate test for recognition rates of neutral
found to be at ceiling both at the immediate (98.5%) and delayed
words to be higher than those of arousing words, and (98%) tests, suggesting that participants were indeed engaged with
there was marginally better recognition of arousing words the central task. Recognition scores of 4 participants who recog-
300 SHAROT AND PHELPS
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70
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orr
C 65 65
n 64.5
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g 60
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% 55 56.25
50
Immediate Test 24-h Delay Test
Neutral Words Arousing Words
Figure3. Experiments 1 and 2: Collapsed recognition rates for peripheral words at immediate
and delayed tests. Brackets represent standard errors of the means.
nized fewer than 14 of the 16 (87.5%) central words correctly were tention of that stimulus than there is of a neutral stimu-
not used (see Method section of Experiment1 for reasoning). lus. Also consistent with Experiments 1 and 2, neutral
words were recognized better at immediate test than at
Results delayed test, suggesting in this case that any arousal caused
Data analysis was the same as in Experiment 1 (see by the central word did not have an enhancing effect on
Results section of Experiment1). retention of the peripheral neutral word. In contrast to
Recognition scores for peripheral words did not reveal Experiments 1 and 2, no crossover interaction of word
a significant interaction of word category (neutral vs. category (arousal vs. neutral) (cid:1) retention interval was
arousing)(cid:1)retention interval [F(1,48)(cid:4)2.41, p(cid:4).127]. found (see Figure4).
The results of a within-subjects ttest indicate that after Interestingly, the results of Experiment3 reveal a nu-
24h, but not immediately, recognition of arousing words merically higher recognition rate for arousing words than
was significantly higher than that for neutral words for neutral words at immediate test, rather than a lower
[t(24) (cid:4) 2.97, p (cid:3) .01]. An independent sample t test recognition rate, as in Experiments 1 and 2. It seems that
shows that recognition for neutral words was better at the the presence of an arousing word at the locus of attention
immediate test than at the delayed test, where recognition throughout all trials in Experiment 3 had a distinct im-
rate was at chance [M(cid:4)49.5%, t(48)(cid:4)2.575, p(cid:3).025]. mediate beneficial influence on memory for the periph-
Recognition for arousing words at the immediate test did eral arousing words relative to the peripheral neutral
not differ from recognition at the delayed test. words.
When the results of Experiment3 were compared with One possible explanation for this trend is the effect
those of Experiment1, no three-way interaction (time of theory (Hochberg, 1978; Neisser, 1976), which states that
test (cid:1)type of word at periphery (cid:1)type of word at cen- the greater congruency a stimulus has with the internal
ter) was found, nor was a main effect of type of central context of the system, the more processing it will re-
word found. ceive; thus, the arousing peripheral word received more
processing than did the neutral peripheral word, because
Discussion it matched the central word both emotionally and se-
In Experiment3 an arousing word, instead of a neutral mantically. The word at fixation set a specific semantic
word, was placed at the center of the screen. In accord and arousing context on all the trials, which enhanced
with results of Experiments1and2, whereas recognition processing for the arousing peripheral word, leading in
for neutral words decreased over time, recognition for turn to better immediate memory. An alternative account
arousing words remained unchanged, and higher recog- of this trend concerns the match between the state of the
nition rates for arousing peripheral words than for neu- participant at times of study and test. It is suggested that
tral peripheral words were revealed at delayed test. These people recollect more accurately when they are in the
results suggest that even when the processing of an arous- same internal state at test as at study (see Balch, Myers,
ing stimulus occurs while overt attention is focused on a & Papotto, 1999 for a review). In Experiment3, the par-
task in a different location, there is better memory re- ticipants processed arousing words at fixation during en-
HOW AROUSAL MODULATES MEMORY 301
coding on all trials, but at test they were presented with As in the previous experiments, recognition of central words was
arousing stimuli only when asked to recognize the emo- found to be at ceiling both at the immediate (99%) and delayed
tional words. Thus, a greater internal state match be- (99%) tests, suggesting that the participants were indeed engaged
with the central task. Recognition scores of 4 participants who rec-
tween study and test, which boosted memory perfor-
ognized fewer than 14 of the 16 (87.5%) central words correctly were
mance, took place on trials testing the arousing words
not used (see Method section of Experiment1 for reasoning).
than on those testing the neutral words.
Results
EXPERIMENT4
Data analysis was the same as that in Experiment 1
(see Results section of Experiment1).
In Experiments 1–3, we examined memory for words There was no interaction of arousal condition (cid:1)reten-
at the visual field periphery, which were either neutral or
tion interval. The 95% confidence intervals for recognition
arousing. These words were presented with either neutral
rates at the immediate test for neutral peripheral words
(Experiments 1and2) or arousing (Experiment3) words presented both in the arousing condition (µ (cid:4)54.87%)
at fixation. In Experiment4, we asked whether the differ- and neutral condition (µ (cid:4)55.18%) slohwoewr that these
ence in forgetting rates, found in Experiments1and2 for lower
rates were significantly different from chance (50%), but
peripheral arousing and neutral words, would originate
they were not significantly different from chance at the de-
only when arousal differences were due to properties of the layed test (µ (cid:4)47.37% and µ (cid:4)44.18%, respec-
actual peripheral stimuli, or whether such differences would lower lower
tively). All pairwise comparisons were found to be not
be found on the basis of arousal changes in the central
significant.
stimuli. In Experiment4, we studied memory for neutral
words presented in the periphery, when eithera neutral or
Discussion
arousing word was presented at the center of the screen.
In contrast to Experiments1 and2, Experiment4 did
The design of Experiment4 was analogous to those of not reveal an interaction of arousal condition (cid:1) reten-
previous studies examining memory for visually periph-
tion interval (see Figure 5), nor were recognition rates
eral details of an arousing event. These studies ordinar-
for words in the arousing versus neutral conditions found
ily place either an arousing or a neutral stimulus in the
to differ at delayed test. These results suggest that the
center of the visual field and a neutral stimulus in the pe-
different forgetting rates for arousing and neutral stimuli
riphery (e.g., Burke et al., 1992; Christianson, 1984;
apparent in Experiments1and2 occur only when arousal
Christianson & Loftus, 1991;Wessel etal., 2000). Some
differences are due to properties of the word tested, and
of these studies, in accord with Easterbrook’s (1959)
not when arousal conditions differ due to elements outside
“narrowing of attention” hypothesis, have reported im-
this stimulus, as when the arousal was due to the central
paired memory for peripheral information in the arous-
word.
ing trials, compared with the neutral trials (Christianson
Presenting either a neutral or an arousing word in the
& Loftus, 1991; Loftus et al., 1987). However, others
center of the screen did not have a significant influence
have not found such an impairment (e.g., Wessel et al.,
on memory of the neutral peripheral word. These find-
2000)—including a study in which eye fixation was con-
ings are consistent with previous studies, which have re-
trolled by brief exposure times (Christianson et al.,
ported no decrement for memory of neutral peripheral
1991). All of these studies tested memory only immedi-
details for arousing versus neutral conditions (Wessel
ately after encoding. One exception is the study by Burke
et al., 2000) when overt attention is controlled (Chris-
et al. that examined memory for such details both im-
tianson etal., 1991).
mediately and after a delay. They found an initial disad-
vantage for memory of peripheral details in the arousing
GENERAL DISCUSSION
condition versus the neutral condition, which decreased
at delayed test.
Arousal may enhance memory by affecting perception
and attention during encoding (Christianson & Loftus,
Method
1991; Reisberg & Heuer, 1992) and by altering memory
Participants. The participants were 50 undergraduates at New
retention (Kleinsmith & Kaplan, 1963; McGaugh, 2000).
York University (31 females and 19 males between 18 and 28 years
of age) assigned to either the immediate test condition (n(cid:4)25) or In this study, we attempted to examine the influence of
delayed test condition (n= 25). arousal on memory, while minimizing the selective mod-
Materials. Materials were the same as in Experiments1,2, and 3. ulation of attention by arousal. The main finding from
Design and Procedure. The method for Experiment4 was iden- our study is that arousal can facilitate slower forgetting,
tical to that of Experiment1 except for two changes. First, at the even when overt attention is not focused on the arousing
center either an arousing word (8 trials) ora neutral word (8 trials)
stimulus. Whereas recognition of neutral words became
was presented (rather than only neutral words, as in Experiments1
worse over time, recognition of arousing words either
and 2, or only arousing words as in Experiment3). Second, in the
periphery onlyneutral words were presented (rather than either neu- stayed the same or showed improvement. A reliable word
tral or arousing as in Experiments 1, 2, and 3). type (arousing vs. neutral) (cid:1)retention interval crossover
302 SHAROT AND PHELPS
75
70 69
ct
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orr 65 64.5
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niti 60
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o
ec 55
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%
50
49.5
45
Immediate Test 24-h Delay Test
Neutral Words Arousing Words
Figure4. Experiment 3: Recognition rates for peripheral words at immediate and delayed tests.
One word (either neutral or arousing) was presented at the periphery at the same time as an arous-
ing word was presented at the center of the screen. Brackets represent standard errors of the means.
interaction, like that reported by Kleinsmith and Kaplan, at immediate test. However, such a difference was not
emerged for the results of Experiments 1 and 2. Results observed.
from Experiments 1–3 show that at the delayed test, pe- Also, in accord with past studies reporting no differ-
ripheral arousing words were remembered better than pe- ence for memory of neutral peripheral details for arous-
ripheral neutral words. Better memory for arousing words ing versus neutral conditions (Christianson etal., 1991;
than for nonarousing words was evident only at delayed Wessel et al., 2000), and contrary to the predictions of
test, supporting the notion that this result was primarily the “narrowing of attention” theory (Easterbrook, 1959),
due to an effect of slower forgetting. Had there been any presenting either a neutral or an arousing word at the
possible confounding properties of the stimuli such as focus of attention in Experiment4 did not alter memory
imageability, concreteness, or frequency underlying these of the neutral words at the visual field periphery. The im-
results, one would have expected to see superior memory plications of this result, as well as those of findings from
for arousing stimuli compared with nonarousing stimuli Experiments 1–3, for theories of the effects of arousal on
75
70
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on 65 63
gniti 62
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%
55
54.5
52
50
Immediate Test 24-h Delay Test
Neutral Condition Arousing Condition
Figure5. Experiment 4: Recognition rates for peripheral words at immediate and delayed tests.
A neutral word was presented at the periphery at the same time as either a neutral or an arousing
word was presented at the center of the screen. Brackets represent standard errors of the means.
HOW AROUSAL MODULATES MEMORY 303
attention and consolidation are considered below, fol- which do not reveal any differences in recognition rates
lowing a discussion of the effects of arousal on the rate of for neutral peripheral words presented with either an
forgetting and on word recognition at the immediate test. arousing or a nonarousing word as the focus of attention,
suggesting that the results of Experiments 1–3 are stim-
Effects of Arousal on the Rate of Forgetting ulus specific and that in this paradigm a general arousal
Consistent with previous findings, indicating that arous- state does not facilitate retention of nonarousing stimuli.
ing stimuli are retained better than nonarousing stimuli This notion is also supported by the results of Experi-
(e.g., Cahill etal., 1996; Canli, Desmond, Zhao, & Gab- ment3, in which presenting an emotional word in the cen-
rieli, 2002), data from Experiments 1–3 revealed that ter of the screen did not seem to facilitate forgetting rates
whereas recognition for neutral words decreased over time, for the neutral peripheral words. Furthermore, in Experi-
recognition for arousing words remained unchanged. After ment2 a peripheral neutral word was presented together
a delay, arousing words were recognized better than neutral with a peripheral arousing word on each trial, but a fast
words. These results go beyond those of previous studies forgetting rate for the former was none the less observed.
in indicating that slower forgetting of arousing words oc-
curs even when that stimulus is presented in the visual field Effects of Arousal on Recognition at the
periphery. Immediate Test
We suggest that one can account for these findings by In all four experiments, no significant difference was
referring to theories of enhanced memory consolidation found between recognition rates for arousing and nonarous-
for arousing stimuli (McGaugh, 1992). Different physio- ingwords at the immediate test. However, a trend was re-
logical systems, including those involved in the discharge vealed of poorer recognition rates attheimmediate test
of hormones believed to affect memory consolidation for arousing words than for neutral words, when data
(Buchanan & Lovallo, 2001; Cahill, 1997; McGaugh, from Experiments1 and2 were collapsed. Although this
2000), become active during, and closely following, the effect is weak, it is consistent with the initial report of
occurrence of arousing events. The influence of arousal Kleinsmith and Kaplan (1963) and with later replications
on enhanced memory consolidation will become evident of this finding (e.g., Baddeley, 1982; Levonian, 1966;
only after a delay, as consolidation of memory happens Walker & Tarte, 1963). Kleinsmith and Kaplan accounted
over time. If memory for arousing stimuli were affected for their counterintuitive result by referring to Walker’s
by arousal, solely by way of strengthening consolidation, (1958)“action-decrement” consolidation theory. The ac-
we would anticipate better memory for such stimuli rela- tion decrement is a refractory state that follows perfor-
tive to neutral stimuli after a delay, but not immediately mance of a response, correlating with the amount of learn-
after encoding. These indeed were our observations. ing that has accumulated to that same response over time.
There are two alternative interpretations of our find- The superior consolidation due to high arousal is advan-
ings. One is that differential covert shifts of attention in tageous over time, but it produces a more intense refrac-
favor of the arousing words may have facilitated the pro- tory state in immediate tests. Thus, information learned
cessing of those words. Although in Experiment2 we at- under high arousal is relatively inaccessible at early test.
tempted to minimize differential covert shifts of atten- Another explanation for Kleinsmith and Kaplan’s
tion by simultaneously exposing participants to both an (1963) finding was put forward by Revelle and Loftus’s
arousing word anda neutral word at the periphery, we do “tick-rate hypothesis” (Revelle, 1989; Revelle & Loftus,
not claim to have eliminated any possible influence of 1990). Revelle and Loftus suggest that arousal increases
such selective shifts on performance. A second alterna- the rate at which a scene is sampled, interfering with ac-
tive hypothesis relates to the level-of-processing frame- cessibility in immediate memory. However, an increase
work (Craik & Lockhart, 1972). According to such an in the rate at which the to-be-learned material is linked
interpretation, although the attentional resources allo- with internal and external context may also aid long-term
cated to each word type in this paradigm may be similar, retrieval. In our experiments, differential sampling rates
a more elaborate encoding of the arousing words could are believed to be minimized by brief stimulus exposure.
lead to enhanced long-term memory. However, both of Thus, although differential sampling rates may carry
these alternative hypotheses would predict better mem- some weight, it seems that this account cannot provide a
ory for arousing words than for neutral words both at the congruous interpretation for this portion of our results. A
immediate test and at the delayed test. It is possible that recent study also suggests that decrements in immediate
some type of inhibition or interference effect was pres- memory for stimuli preceding emotional items are linked
ent at the immediate test for the arousing words, lower- to amygdala-dependent β-adrenergic modulation of epi-
ing accuracy rates. Possible interference effects at the sodic encoding (Strange, Hurlemann, & Dolan, 2003).
immediate test are discussed in the next section. The results of some studies (Doerksen & Shimamura,
The differences in forgetting rates (Experiments1–2) 2001) imply that the lack of memory enhancement by
and the differences in recognition rates at the delayed test arousal at immediate test may be specific to cued recall
(Experiments 1–3) for neutral and arousing peripheral and recognition tests (Richardson, Strange, & Dolan,
words do not occur when arousal conditions differ be- 2004) rather than to free recall (Strange, Henson, Friston,
cause of the central word, rather than the tested periph- & Dolan, 2000). To date, the specific neural and cogni-
eral word. This is implied by the results of Experiment4, tive mechanisms underlying the decrement for immediate