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| Volume 5, Number 3, Article 6, Pages 215-229 |
doi:10.1167/5.3.6 |
http://journalofvision.org/5/3/6/ |
ISSN 1534-7362 |
Short-term memory for scenes with affective content
Vera Maljkovic |
Department of Psychology, The University of Chicago, Chicago, IL, USA |
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Paolo Martini |
Department of Psychology, Harvard University, Cambridge, MA, USA |
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Abstract
The emotional content of visual images can be parameterized along two dimensions: valence (pleasantness) and arousal (intensity of emotion). In this study we ask how these distinct emotional dimensions affect the short-term memory of human observers viewing a rapid stream of images and trying to remember their content. We show that valence and arousal modulate short-term memory as independent factors. Arousal influences dramatically the average speed of data accumulation in memory: Higher arousal results in faster accumulation. Valence has a more interesting effect: While a picture is being viewed, information from positive and neutral scenes accumulates in memory at a constant rate, whereas information from negative scenes is encoded slowly at first, then increasingly faster. We provide evidence showing that neither differences in low-level image properties nor differences in the ability to apprehend the meaning of images at short exposures can account for the observed results, and propose that the effects are specific to the short-term memory mechanism. We interpret this pattern of results to mean that information accumulation in short-term memory is a controlled process, whose gain is modulated by valence and arousal acting as endogenous attentional cues.
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History
Received September 14, 2004; published March 18, 2005
Citation
Maljkovic, V. & Martini, P. (2005). Short-term memory for scenes with affective content.
Journal of Vision, 5(3):6, 215-229,
http://journalofvision.org/5/3/6/,
doi:10.1167/5.3.6.
Keywords
visual short-term memory, emotions, IAPS, RSVP, image statistics, attention
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Visual short-term memory (VSTM) plays a crucial role in
what we colloquially call “seeing.” A dramatic demonstration of this
memory limit to the conscious appreciation of visual scenes was given by Molly
Potter in a series of now classic studies (Potter, 1975; Potter, 1976; Potter & Levy, 1969). By using the Rapid Serial Visual
Presentation Procedure (RSVP), she showed that short-term recall of pictures
seen briefly within a continuous stream could be very poor, yet a cued search
for a particular item within the stream remained efficient even when the
pictures were seen for only 125 ms each. Evidently, enough visual processing
takes place within such a short temporal window to allow the efficient
recognition of a template object defined by abstract instructions. However, the
fast alternation rate of the RSVP stream exceeds the limit for encoding in a
more permanent memory store, making impossible the recall of the contents of the
scene during a subsequent memory recognition stage. As such, the experiments of
Potter and later those of many others (Coltheart, 1999) have shifted the focus of attention to
short-term memory, as opposed to early visual mechanisms, as the real bottleneck
of conscious vision. Even more crucial must be the role of short-term memory in
the visual interpretation of scenes with affective content, because in many
conditions emotional content mandates a response from the organism. Yet, almost
nothing is known of how emotions and visual short-term memory interact in
guiding behavior. Only a handful of studies have looked at the influence of
emotion on short-term memory, with controversial results. Some authors deny any
selective effects of emotions on STM (Bianchin, Mello e Souza, Medina, &
Izquierdo, 1999; Izquierdo, Medina,
Vianna, Izquierdo, & Barros, 1999;
Quevedo et al., 2003). However, at least
two recent studies provide hints as to possible emotional effects on VSTM and/or
attention (Anderson & Phelps, 2001;
Kensinger & Corkin, 2003). In
contrast, the influence of emotional content on encoding and retrieval is well
characterized for long-term memory: Emotionally charged information is encoded
and retrieved more efficiently than emotion-neutral information (Hamann, 2001), and the role of the amygdala in this
context has been particularly well studied (Cahill & McGaugh, 1998; Klüver & Bucy, 1937; McGaugh, McIntyre, & Power, 2002).
Beginning with Wundt ( 1916), it has been recognized that the emotional
experience varies along two principal, independent axes: valence, or degree of
pleasantness, and arousal, or intensity of the evoked emotion (Lang, Bradley,
& Cuthbert, 1990; Osgood, Suci, &
Tannenbaum, 1957; Russell, 1980). Following such a model, the emotional
quality of any stimulus can be classified by asking observers to rate the
stimulus on appropriate scales along the two dimensions (valence and arousal)
and reporting the obtained scores as the coordinates of a point in a cartesian
plot (see Figures 1 and 2). In the present study, we have investigated
the temporal dynamics of information accumulation in short-term memory for
real-life scenes with affective content varying in valence and arousal. We
propose a simple model ( Memory model) of
the dynamics of information accumulation in VSTM during an RSVP task and
demonstrate that its independent parameters are modulated orthogonally by
valence and arousal ( Experiment 1). From
this we argue that arousal and valence must act as largely independent factors
on VSTM. Arousal modulates the time constant of the memory accumulation process
for both negative and positive valence images. In contrast, the effect of
valence is specific for negative images and consists of a progressive
acceleration of information accrual with increasing image exposure. We provide
evidence that such valence effects are unlikely to be due to trivial differences
in image statistics ( Image statistics) or
to greater difficulties of semantic categorization at short exposures for
negative valence images compared to positive ones ( Experiment 2). Finally, we show that the
effects observed are most probably specific to the memory mechanism, because
they are not found in a recognition task where memory load is thought to be
minimal ( Experiment 3).
Figure 1. Valence and arousal scores of
images from the IAPS picture set. Each image in this standard set has been rated
for the degree of pleasantness (valence) and for the intensity of the perceived
emotion (arousal). The subset of the pictures used in the experiment is
indicated by the colored symbols.
Figure 2. Example pictures from the IAPS
set. The images represent the combinations of arousal and valence categories
used in the experiments. The lowest arousal images (here the iron, man at
window, file cabinets, and basket) were used as buffers and never tested for
recall.
The main dependent variable in our study is the
fraction of pictures recognized as function of exposure time. We take this
fraction to represent the probability that a given picture will be remembered
when seen for a given exposure within the RSVP stream. As will be seen in the
data, cumulative recognition probability increases monotonically with exposure,
presumably reflecting the accumulation of information extracted from the
stimulus and stored in memory.
We assume that following the stimulus’ appearance
a number of symbolic representations are formed, embodied in the neural
responses to various features of the stimulus. The information represented in
these various neural activities competes for access to a temporary memory store,
where a cumulative representation of the stimulus at hand is being formed. We
envisage such information accumulation process as a form of sampling with
replacement. Due to capacity limitations, within a given temporal bin only a
fraction of the total stimulus information is accessed. Because sampling is with
replacement, the incremental gain of stored information per unit time will be
large immediately after the stimulus onset and will subsequently diminish due to
repeated re-sampling of identical bits of information. This incremental
information gain is reflected in the increasing cumulative probability of a
correct response with increasing exposure.
We seek to formalize in terms of a probability the act
of sampling and storing in memory a limited amount of information per unit time.
The concept of hazard rate is the most
appropriate for this task (Luce, 1986; Ross,
2003). The hazard rate of information
accumulation in memory is the conditional probability that a bit of information
never sampled previously is sampled and stored in the current unit of time. In
the context of the RSVP experiment, the hazard rate can be taken to indicate the
probability that a picture will be correctly remembered if seen for an extra
instant of time, having failed to be remembered when seen for a shorter
time.
The hazard rate
h(t)
can be expressed
as  | (1) |
where
f(t)
is the probability density and
F(t)
the distribution function [the quantity
1− F(t)
is often referred to as the survival
rate and its logarithm as the log
survivor function]. If the form of the hazard function is known, then the
distribution function can be derived analytically by integrating Equation
1:  | (2) |
Consider the case of a constant hazard rate:
 | (3) |
In such a case the distribution function
becomes  | (4) |
This is the familiar exponential function, which has
been used to model the results of short-term memory experiments in many previous
studies (Bundesen & Harms, 1999;
Lamberts, Brockdorff, & Heit, 2002;
Loftus & Ruthruff, 1994; Shibuya &
Bundesen, 1988).
However, there is no a priori reason to assume a
constant hazard rate: Information accumulation could accelerate or decelerate
over time, necessitating a model able to accommodate increasing or decreasing
hazard rates. Consider then the following hazard
function:  | (5) |
Here, the hazard rate decreases, remains constant, or
increases in time with choices of β
< 1, β = 1,
β > 1, respectively. The
corresponding distribution
function  | (6) |
is the well-known two-parameter Weibull function. Note
that when expressed as
log(t),
the function changes scale (shifts laterally on the
x-axis) but not shape (steepness) with
changes in α, whereas it changes
shape but not scale with changes in
β. We adopt Equation 6 as our model for the accumulation
of data in short-term memory. While our choice is dictated by the necessity to
allow for a range of hazard rates and by the ease with which such property is
embedded in a single parameter in the case of the Weibull function, such a
choice might have a deeper justification if it were possible to demonstrate that
data accumulation in memory can be described as an extremal process, in which
case the Weibull would be the appropriate limiting distribution (Kotz &
Nadarajah, 2000).
General materials and methods
Subjects were students at The University of Chicago,
aged 18-25 years, naïve to the purpose of the experiments, without prior
exposure to the image set, and with both sexes equally
represented.
The International Affective Pictures System (IAPS) set
(Lang, Bradley, & Cuthbert, 1999) of 384
color images was shown to each subject in each task, each image only once per
subject. The images were chosen to represent a variety of combinations of all
possible arousal and valence levels, clustered as shown in Figures 1 and 2 to facilitate experimental counterbalancing
and subsequent data analysis. All images subtended 8 x 10 deg of visual angle
(when the size and/or aspect ratio of the original IAPS images differed from
such template, they were cropped and scaled as needed), and were presented
surrounded by a black background on a computer monitor at a refresh rate of 75
Hz. The experiments took place in a dimly lit room. Subjects entered their
responses on the computer keyboard. The presentation procedures were programmed
in-house on an Apple G3 computer using C and the VisionShell routines by Raynald
Comtois (Comtois, 2000-2003).
The RSVP task consisted of 24 self-paced consecutive
trials during which each subject was exposed to the entire stimulus set. On each
trial (see Figure 3 for an example), subjects
were shown a 10-image stream, followed after a 1.5-s blank delay by a test phase
in which 16 pictures where shown singly, 8 new and 8 old randomly interspersed.
To eliminate primacy and recency effects, each stream began and ended by a
neutral, very low arousal image, and these images were never tested for recall.
Within each stream, images appeared for a set exposure (ranging from 13 ms to 4
s) and without interruption between successive frames. During the test phase,
each test picture stayed on the screen until the subject indicated whether it
belonged to the previously seen stream. Two practice trials (not entered into
the final analysis) preceded 24 experimental trials. Each subject was tested at
4 different exposures, for a total of 96 subjects over 15 exposures.
Figure 3. Schematics of the RSVP
procedure. In the study phase the subject sees a stream of 10 pictures shown
back-to-back. After an ~1.5-s interval, the test phase commences where 16
pictures (8 old, 8 new) are shown singly, requiring the subject to indicate
whether the picture s/he is looking at was present in the study stream.
To ensure a maximal degree of randomization, the
experimental design was carefully constructed according to several
counterbalancing rules. Within the limits imposed by the high dimensionality of
the parameters’ space, the pseudorandom design matrix thus minimized the
chances that the results were contaminated by properties of individual images,
serial presentation and serial testing position, combinations of particular
images, predictability of the upcoming arousal/valence category, and primacy and
recency effects.
Previous pilot rating experiments had indicated that at
long exposures arousal and valence rating scores obtained from the subject
population of the current study were very highly correlated to the normative
IAPS scores
( rarousal=.72;
rvalence=.94).
Subjects’ responses from the RSVP task were then parsed into eight arousal
categories (arousal ratings 3-3.5, 3.5-4, 4-4.5, 4.5-5, 5-5.5, 5.5-6, 6-6.5, and
> 6.5) and seven valence categories (valence ratings 1-2, 2-3, 3-4, 4-5, 5-6,
6-7, and > 7) according to the normative ratings of the IAPS set. Within each
category, proportion correct recalls were calculated at each exposure. The
scores were corrected for guessing by subtracting the false alarm rate from the
hit rate. Scores never reached 100% correct even at the longest exposures: The
errors were interpreted as lapses of attention or random errors in motor
choices. As none of these factors were the focus of the experiment, they were
removed by normalizing the corrected-for-guessing scores to the asymptotic
value, taken as the average score at the two longest exposures (in all cases 95%
or better). Scores were then fitted by nonlinear regression with a two-parameter
Weibull function of the form indicated in Equation 6. All reported fits corresponded to
R2 > .96. To obtain
non-parametric estimates of hazard rates, probability densities were calculated
from the cumulative scores and then divided by the survival rates (as detailed
in Results).
This experiment revealed two effects: (1) Valence
(pleasantness) and arousal (intensity of the evoked emotion) independently
affect memory accumulation, and (2) recognition memory for negative images
demonstrates an increasing hazard rate, whereas memory for neutral and positive
images follows a constant hazard rate. An illustrative summary of these findings
is presented in Figure 4, which shows the
measurements and associated best-fitting Weibull functions for the two extreme
arousal and valence categories. In the arousal graph, subjects’ scores
where averaged across all valence categories; conversely, in the valence graph,
subjects’ scores were averaged across all arousal categories. In
semi-logarithmic coordinates (proportion remembered vs. log time), increasing
arousal shifts the curve leftward (decreases α) signifying overall improvement
in performance, whereas a change from positive to negative valence increases the
slope of the curve (increases β),
indicating a progressive acceleration of correct response accumulation as
exposure increases.
Figure 4.
Results from the RSVP task. On the left, correct response curves for images
belonging to all valence categories with arousal values 3-3.5 (mean arousal
3.31) and > 6.5 (mean arousal 6.84), showing that arousal affects performance
by shifting the psychometric function laterally in log time. On the right,
response curves for images belonging to all arousal categories with valence <
2 (mean valence 1.84) and > 7 (mean valence 7.38), showing that valence
affects performance by changing the slope of the psychometric function, but not
its location on the log time axis. Continuous curves are best-fitting Weibull
functions ( Equation 6). Each data point
represents the proportion of correct responses averaged across subjects at that
image exposure, corrected for guessing and lapse rates.
The subjects’ behavior across all arousal and
valence categories can be parameterized by expressing the results in terms of
the Weibull model’s α and
β values, as shown in Figure 5. The α values show a linear
correlation with arousal ( r =
−.71, n = 8,
p < .047), but do not correlate with
changes in valence ( r = −.00004,
n = 7,
p < .999). Conversely,
β values
correlate significantly with valence ( r
= −.87, n = 7,
p < .01), but are constant as a
function of arousal ( r = .04,
n = 8,
p < .92). Notice that there are also
clear nonlinear trends in the data: For example, in Figure 5, the
α/arousal graph seems to asymptote
to a constant level and the
β/valence graph might be
interpreted as a step function. These higher order trends could be the result of
uneven sampling, the nonuniform coverage of all valence and arousal categories
in the image set, or more specific factors affecting each particular condition.
Nonetheless, the first-order, linear approximation is an important and robust
generalization, and overall the pattern of results suggests that arousal and
valence operate independently.
Figure 5. Results from the RSVP task. The
α (location parameter) and β
(slope parameter) of the best-fitting Weibull curves are shown on the left for
all arousal categories averaged over valence categories, and on the right for
all valence categories averaged over all arousal categories. The dashed lines
represent 95% confidence intervals of the estimates.
α correlates (negatively) with
arousal, but not with valence; conversely, β correlates (negatively) with
valence, but not with arousal.
To independently assess the differences in the
responses to the valence categories, without the potential contaminating
constraints introduced by the parametric modeling of the data, we also
calculated hazard rates directly from the observed scores, as indicated in Equation 1. The results, shown in Figure 6, indicate that indeed the responses to
neutral and positive images display a constant hazard rate, whereas the hazard
for negative images accelerates over time, particularly during the first 500 ms
of exposure. Thus, the nonparametric analysis confirms the results of the
parametric modeling, indicating that negative images are treated differently
than neutral or positive ones.
Figure 6. Hazard
rates for images with valence 1 to 4 (negative), 4 to 6 (neutral), and 6 to 9
(positive), averaged across arousals in the RSVP task. The rate for negative
images increases with exposure, whereas that for positive and neutral images is
virtually constant. Symbols indicate data derived from the proportion correct
scores. Solid lines are linear regressions of log hazard rates on log time (only
the coefficient for the negative images is statistically significant,
bnegative=.001, p < .001;
bneutral=.00005,
p <,.75;
bpositive=.00005,
p < .60).
Notice also that the mean hazard rate for neutral
images is lower than for positive images, corresponding to a longer time
constant. The same trend is also found in the parametric estimates (see Figure 5, top-right panel), where the average
α
value for neutral images is higher than for positive images. This
difference is likely due to a sampling problem inherent in the structure of the
image set, which introduces a spurious interaction between valence and arousal:
Neutral images, compared to positive ones, lack high arousal content (as can be
seen in Figure 1). Indeed, such a difference
disappears if the responses to low arousal positive images are compared to the
neutral ones. A similar interaction is present also for negative and positive
images: On average, negative images, compared to positive ones, are scored
higher in arousal. However, the analysis of subsets containing only
low-arousal/negative (mean arousal=4.47) and only high-arousal/positive (mean
arousal=5.80) pictures indicates that negative images have a slope significantly
higher than unity ( β =
1.30, CI = 1.13–1.48), whereas
positive images do not deviate significantly from unity
( β = .96, CI = .88–1.03).
This suggests that differences in slope cannot be accounted for by biases in the
sampling of arousal
levels.
Improved performance with increased arousal may relate
to increased alertness or a better sensory quality of the stimulus. Changes in
arousal may affect the availability of processing resources or the magnitude of
the sensory response, thus changing the amount of information made available per
unit time. The effect of arousal can then be interpreted as modulating the time
constant of the accumulation process, similar to the fast changes in gain
induced by increasing image contrast (Loftus & Ruthruff, 1994; Stromeyer & Martini, 2003) or brightness (Kelly, 1961). Thus arousal modulates the
α parameter of the Weibull
model.
What about the
β parameter? The results of
similar RSVP tasks have been previously interpreted within the framework of a
conceptual short-term memory system (Potter, 1976). Current models of conceptual short-term
memory (Bundesen & Harms, 1999;
Lamberts et al., 2002; Loftus & McLean, 1999; Shibuya & Bundesen, 1988) postulate that the proportion of correct
responses at any given image exposure is equivalent to total information
acquired in memory. According to this class of models, information accumulates
in memory at a constant rate following stimulus presentation, as evidenced by
cumulative frequency of response curves that can be fitted with simple
exponential functions. Our data for neutral and positive images conform to such
models: A β value approaching
unity effectively reduces Weibull curves to simple exponentials.
The rate of correct response accumulation shows,
however, a marked difference for negative compared to positive or neutral
images: It increases with the duration of image exposure, requiring a
β > 1. This effect is best
understood by examining the hazard rates of the responses. An increasing hazard
rate implies that information accumulation in memory
accelerates over time. Neutral and
positive images, which elicit constant hazard rates, appear to be processed in a
manner where each successive state of the system is independent of the previous
states. In probability terms this is equivalent to sampling with replacement and
defines a processing mode that is essentially automatic. Negative images may
instead trigger a more intelligent processing mode whose current state is
influenced by the previous history and thus shows signs of a more controlled
activity. The corresponding hazard rate starts lower, but then increases,
indicating that memory encoding of information from negative images accelerates,
particularly during the first 500 ms of exposure.
We are now facing the question of what is the nature of
the mechanism responsible for such processing differences between images of
different affective value. We examine first the two most immediate explanations,
both based on the observation that negative images are at a disadvantage at the
shortest exposures. Images eliciting negative affect might have poorer physical
image qualities, such as brightness, contrast, and spatial frequency content, or
might require more time to be processed conceptually, a conjecture tested in Experiment 2. The specific contribution of
short-term memory is examined in Experiment
3, and more elaborate accounts are further discussed in General Discussion.
An extensive examination of the contribution of
low-level image properties to the categorization of emotional images will be
described elsewhere (for a preliminary report, see Maljkovic, Martini, &
Farid, 2004). Here we provide a brief
report examining basic image properties that might differ between valence
categories, thus potentially forming the bases for the differential effects of
valence on memory accumulation.
The 384 images from the IAPS set were analyzed for mean
luminance, contrast, and spatial frequency differences. The mean (related to
mean-luminance) and SD (related to
contrast) of the intensity of all pixels across each image were calculated
separately for each RGB color component and for their linear sum. The spatial
frequency power spectrum was also extracted from a grayscale version of each
image, and the obtained series of frequency coefficients was fitted with a power
function of the
form  | (7) |
where
f is spatial frequency and
λ a coefficient related to the
high-frequency cut-off of the spectrum. A lower power coefficient
λ indicates that the image
contains more high-spatial frequencies relative to an image with a higher
exponent. Pair-wise correlations were computed
between the obtained mean intensity,
SD, and power coefficients of each
image and its arousal and valence normative rating. Only mean intensity and
power significantly correlate (p <
.05) with valence
(rintensity=.12,
rpower=–.16,
N = 384), whereas none of the
statistics covaries significantly with arousal.
For each of these image dimensions (mean intensity and
power), two subsets were created comprising images with scores above and below 1
SD of the mean. A Weibull model was
then fitted to the responses given within the RSVP task to each subset, yielding
a comparative estimate of the model’s parameters across dimensions.
Pictures with high- and low-power exponent
λ showed no difference in either
Weibull’s parameter
( αlow = 371, CI
319-423; βlow = 1.08,
CI .87-1.29; αhigh =
332, CI 287-377; βhigh
= 1.11, CI .9-1.32). High- and low-brightness images, on the other hand, did
produce a difference in the α
parameter, brighter images being recognized better at faster exposures than
darker images
( αbright
= 278, CI 255-301;
βbright = 1.02, CI
.91-1.13; αdark = 424,
CI 383-465; βdark =
1.17, CI 1-1.34). Correlation and RSVP data for the mean intensity partitions
are shown in Figure 7.
Figure 7. Effect of mean pixel intensity on RSVP
performance. A. Each of the 384 IAPS images used in the experiment is
represented by a standardized score for mean pixel intensity and valence rating;
the red line is a linear regression of the statistic on valence
(r = .12). B. Mean intensity histogram
of the image set. C. Weibull fits to the RSVP responses to images 1
SD above and below the mean of the
statistic (shaded areas in A and B).
A three-fold difference in mean-luminance corresponds
to a difference of ≈150 ms in average speed of information accumulation in
the RSVP task (α parameter), but
does not significantly affect the steepness of the curves
(β
parameter).
In summary, no positive finding has emerged from the
study of the interactions between image statistics and emotional responses.
Basic luminance statistics correlate very weakly with the emotional dimensions.
An appreciable effect on the RSVP responses can be observed only for large
differences in mean pixel intensity, paralleling the effects observed with
variances in arousal. Yet, there is no obvious correlation between arousal
ratings and the mean luminance of images. While the role of low-level image
properties needs to be explored more deeply, it is hard to avoid the conclusion
that the image statistics analyzed so far do not drive the results obtained in
the RSVP task, particularly as regards differences in the steepness of the
curves.
Experiment 2: Valence-rating task
In the RSVP task of Experiment 1, negative images were
remembered less than positive or neutral images when presented at the shortest
exposures. It is possible that negative images require longer times to be
comprehended conceptually, thus explaining the reduced performance and the
effect on the steepness of the psychometric curves. This conjecture was tested
in the present experiment by examining the ability of observers to categorize
images at all
exposures.
The valence-rating task consisted of 384 consecutive,
self-paced trials during which each subject was exposed to the entire IAPS set.
On each trial subjects saw a single image followed by a nonsense, color, noise
mask (see Figure 8). The mask consisted
of a static checkerboard, where each square check had a size of 0.25 deg and a
color extracted at random from the color palette of the test-mage. Images were
presented for exposures of 13-1710 ms (counterbalanced across trials and across
subjects), while the mask lasted 4 times longer than the test-image. After
seeing each picture/mask combination, subjects rated the valence of the image on
a 9-point scale and indicated the confidence of their rating on a 3-point scale.
The instructions verbally given to the subjects on how to form their response
were as follows: “After you have seen an image, you will be asked to
indicate how pleasant or unpleasant is the situation represented. If the picture
represents a very pleasant situation respond +4; if it represents an extremely
unpleasant situation respond –4. You should rate neutral pictures that are
neither positive nor negative as 0. For intermediate levels of
pleasantness/unpleasantness use intermediate ratings (1 to 3 for pleasant,
–1 to –3 for unpleasant). If the picture was presented so briefly
that you couldn’t see much and therefore you couldn’t make up your
judgment, respond 0. Do not think too long about the rating to give to any
picture. You will then be asked to indicate how confident you are about your
response. You can choose among completely sure, not so sure and totally
unsure.” Each subject was tested on 4 exposures. A total of 48 subjects
were tested over 8 exposures. The experimental design was counterbalanced so
that 6 ratings were collected per image at each exposure from different
subjects.
Figure 8. Valence-rating task. The subject is
presented with an image for a set exposure, followed by a checkerboard color
mask. The response consists of a numerical value attributed to the picture
indicating the perceived degree of pleasantness.
The subjects’ rating of any image was remapped to
the range 1-9 (by adding 5 to each score) and assigned to a negative, neutral,
or positive category, according to the normative valence score of that image
published in the IAPS set. These three categories had valence < 4, 4-6, and
> 6, respectively, averaged across arousal levels. At each exposure the
ratings were averaged across subjects within each category. Hazard rates for
categorization were calculated from the proportion assignment of each image to
its asymptotic category at any image
exposure.
The average ratings of the images given by the subjects
are shown in Figure 9A. Affect builds up with
increasing exposure: Positive and negative images are categorized as such
increasingly more often as the pictures are seen for longer times. However,
already with an exposure of one video-frame, the different categories are
separately clustered, positive images being on average rated higher than neutral
images ( t = 5.39,
p < .001,
df = 1295) and neutral images rated
higher than negative images ( t = 7.08,
p < .0001,
df = 1294). Of specific interest here
is the temporal dynamic of the categorization process: Is there a difference in
the time-course of the semantic valuation of positive as opposed to negative
images? Do negative images take longer to be categorized as such compared to
positive images?
Figure 9. Results from the valence-rating
experiment. A. Average subjects’ ratings showing that reliable
categorization is achieved already at an exposure of only one video frame (95%
CI are smaller than symbols). B. Proportion of correctly categorized images at
each exposure. C. Hazard rates, equivalent to conditional, instantaneous
probabilities of a correct categorization. The rates for positive and negative
images are indistinguishable and decrease over time.
To answer these questions we coded as correct any
response that had assigned an image to the same category as that to which it
belonged, according to the normative, IAPS rating, and as incorrect those
responses that did not correspond to the IAPS rating. For example, if picture Z
was assigned by a subject a rating of 5 while the IAPS rating was 7 (i.e., a
positive picture), the assigned score would be incorrect, because we took
positive pictures to be rated as 6 or higher. We then calculated the proportion
correct scores per exposure for positive and negative images and corrected the
results for guessing (guessing rate was 33%). The final results of this
calculation are shown in Figure 9B. This kind
of analysis reveals no difference in the temporal dynamic of categorization for
positive and negative images: The two curves overlap.
By analogy to the RSVP model, it is tempting to
interpret the proportion correct score as a measure of the accumulation of
stimulus information leading to the semantic categorization of the image.
Following such interpretation, the hazard rate of the categorization process
then indicates the probability that a bit of information not yet extracted from
the stimulus is extracted in the next instant of time and contributes to forming
a semantic valuation of the image. The hazard rates for categorization,
calculated from the proportion correct scores, are shown in Figure 9C. The hazard curves for positive and
negative images overlap, indicating similar temporal dynamics. Interestingly,
both curves have a decreasing excursus and largely fade after 200 ms of
exposure. Contrast this to the constant or increasing trend found in the RSVP
task.
The valence-rating experiment was prompted by the
conjecture that the conceptual meaning of negative images might be harder to
grasp, particularly at the shortest exposures, thereby accounting for the
steeper response curves found in the RSVP task. In favor of this hypothesis is
the observation that images of negative valence tend to be encountered less
frequently in everyday life, therefore lacking in familiarity to the subjects.
Contrary to the hypothesis, we found that with an exposure of only one video
frame both negative and positive pictures are categorized as such at a rate
better than chance. Moreover, examination of the temporal dynamic of the
semantic classification of the scenes revealed that the categorization process
appears to proceed at the same rate for both positive and negative images. This
implies that an early, selective categorization disadvantage for negative images
is not a likely explanation for the effects observed in the RSVP task.
Recent studies (Keysers, Xiao, Foeldiak, & Perrett,
2001; Li, VanRullen, Koch, & Perona, 2002; Thorpe, Fize, & Marlot, 1996; VanRullen & Thorpe, 2001a) have demonstrated very clearly that
several categorization tasks can be successfully performed with very brief
exposures: The present finding extends this ability to the domain of emotional
valence. Yet, it might be argued that the mask we used was not powerful enough
to arrest processing. Indeed, the checkerboard mask contained most of the power
at one spatial scale, was static, and its duration was proportional to the
test-image exposure. However, in follow-up experiments to be described elsewhere
(for a preliminary report, see Maljkovic et al., 2004), we have used multi-scale, dynamic
masks presented for 2 s at all image exposures and have obtained virtually
identical results. Finally, one widely accepted marker for mask effectiveness is
the fact that performance decreases constantly with shorter stimulus onset
asynchrony, as can be seen clearly in the data.
The examination of the temporal dynamic of the semantic
classification revealed a surprising fact: Unlike the RSVP task, in which scene
information keeps accumulating steadily up to 2 s of exposure, the scene
categorization task seems to rely on a more transient response, where most of
the information relevant to the task is extracted very early. This difference is
evident in the pattern of the hazard rates: Hazards are constant or increasing
with exposure for the RSVP task, but peak early, then decline and fade to a very
small value by 200 ms of exposure in the categorization task. It is tempting to
speculate that the different dynamics observed in the two tasks might be related
to the different demands on memory, a conjecture further examined in Experiment
3. Experiment 3: Simultaneous matching-to-sample task
The matching-to-sample task consisted of 192
consecutive, self-paced trials during which each subject saw 192 images from the
IAPS set. On each trial subjects saw a single image presented in the top half of
the screen for exposures of 13-100 ms (counterbalanced across trials and across
subjects). Following the study exposure, the picture was immediately replaced by
a display containing 3 images: The study image was replaced by a picture mask
drawn from an additional set of 192 images of neutral emotional content; in the
lower part of the display the study (“seen”) image reappeared to the
left or right (chosen randomly) of a comparison (“unseen”) picture
drawn from the IAPS set and having similar arousal and valence rating (see Figure 10). These three images remained on the
screen until the subject indicated which picture (lower left or right) matched
the “seen” image. Each picture (seen, unseen, and mask) was
presented only once per subject. A total of 24 subjects were tested over 4
exposures.
Figure 10. Simultaneous matching-to-sample task.
On the left is an example of a trial. The subject’s task is to match one
of the images in the lower part of the display to a study image he/she has seen
earlier for a short exposure and followed by a picture mask. On the right are
results for the three emotional categories, showing no difference in
performance.
Each image was assigned to a negative, neutral, or
positive category, according to the valence score of that image published in the
IAPS set. These three categories had valence < 4, 4-6, and > 6,
respectively, averaged across arousal levels. Within each category, proportion
correct matches were calculated at each exposure across all subjects. The scores
were then corrected for guessing by subtracting chance performance from the
observed fraction correct and dividing by 1 minus chance performance.
As can be seen in Figure 10, performance in this task is very
good: On average, subjects are able to correctly match 40% of the images
(discounting guesses) at only one video-frame exposure and show perfect
recognition with an exposure of 100 ms. No difference can be observed between
the different image categories at any exposure. As such, these results parallel
those obtained in the rating task of Experiment
2. Thus the results of this very simple task and those of the rating task
of Experiment 2 demonstrate that when memory
interference is low the responses to images varying in emotional content are
indistinguishable. This suggests that the differential performance observed in
the RSVP task has to be ascribed to mechanisms that selectively affect
short-term memory
accumulation.
Performance in RSVP tasks is summarized remarkably well
by Weibull models. Perhaps the best way of showing this is to consider Equations 1, 2, and 6
together, leading to the following
expression: | (8) |
Transforming to logarithms obtains the equation
of a
line  | (9) |
whose coefficients can be estimated by linear
regression. Data and model from the RSVP task of
Experiment 1 are thus summarized in Figure 11 using the format of Equation 9. Figure 11. Log survivor plots. The data of the
RSVP experiment for positive, neutral, and negative images are plotted here
according to Equation 9. In such a format
the performance curves are linearized and differences in slope are maximally
evident. Solid lines through the data are best-fitting linear regressions
estimating the Weibull parameters
( β_positive=1.04, CI .98-1.10;
β_negative=1.43, CI 1.35-1.51;
β_neutral=1.00, CI .88-1.12;
α_positive=341, CI 315-369;
α_negative=355, CI 329-381;
α_neutral=381, CI 320-442). Notice
how positive and neutral images follow the dashed line, which has a slope of
unity, whereas negative images are substantially steeper.
The slope of the function (shape, or
β parameter) is unity for positive
and neutral pictures, corresponding to a constant hazard rate, but it is greater
than unity for negative images, indicating that with negative pictures the
hazard rate increases with exposure time. The difference in intercept is also
dependent only on β, as can be
demonstrated by constrained regression with
α as a shared parameter. The scale
parameter α, indicating the
exposure at which 63% of images are remembered, thus does not vary as a function
of valence; however, it does vary with arousal. Across arousal levels it can
differ by as much as 150 ms, as can be seen in Figure 5, and this range of variation is
comparable to what can be obtained with a three-fold difference in the overall
brightness of images (see Figure 7).
Therefore, the parameters of the Weibull model describing recognition memory
performance in the RSVP task correlate orthogonally with valence and arousal:
Shape correlates with valence and scale correlates with arousal, but not
vice-versa. As such, we interpret these results to indicate that valence and
arousal affect short-term memory performance independently.
Osgood et al. ( 1957) was among the first to demonstrate by
factor analysis that valence and arousal are two independent dimensions of the
emotional experience, a fact accepted by many modern psychological theories of
emotions (Lang et al., 1990; Russell, 1980). More recently, several imaging and
electrophysiological studies have demonstrated that dissociable anatomical
substrates are responsible for the effects induced by these two dimensions
(Anderson et al., 2003; Arana et al., 2003; Kensinger & Corkin, 2004; Small et al., 2003; Yeung & Sanfey, 2004). The amygdala is often indicated as the
primary structure involved in arousal-dependent responses, whereas the
prefrontal cortex has been implicated in responses that vary with valence. It is
thus not so surprising that this independence carries also to short-term memory.
The separate influence on performance attributable to
each dimension has intriguing implications. Arousal effects are similar to those
elicited by varying the mean-luminance of images. These effects could be
entirely automatic, perhaps feed-forward and dependent upon the magnitude of
response in the early filters (Loftus & Ruthruff, 1994), or feed-back in nature, such as due to
gain control mechanisms (Wilson & Humanski, 1993), but with very fast temporal dynamics.
Either way, the net result is an essentially instantaneous modulation by arousal
of information uptake, with virtually no evidence that the speed of processing
changes with increasing exposure. However, when confronted with images of
negative valence, subjects’ performance bears the signature of a more
controlled process, demonstrating a clear temporal dynamic. Short-term memory is
impaired at the shortest exposures, but improves faster than for positive images
at longer exposures. The signature phenomenon of this effect is an accelerating
hazard rate. We interpret this pattern of results to mean that information
accumulation in short-term memory is a monitored process, whose gain is adjusted
quickly and automatically as function of arousal, but also actively and
vigorously modified by the realization that an image has negative content.
We propose that the difference observed in the RSVP
task between positive and negative images is specific to VSTM encoding. Three
converging lines of evidence support this claim: Different valence categories
share the same image statistics ( Image
statistics), making it unlikely that the effect observed depends on
low-level image properties; the temporal dynamics of emotional categorization
does not differ across valence categories ( Experiment 2), suggesting that a cognitive
evaluation of the meaning of the scene is available equally early for all
emotional categories; and, finally, tasks such as simultaneous
matching-to-sample ( Experiment 3), which
minimize short-term memory load, do not elicit a behavioral effect specific to
valence.
The luminance statistics of images that we have
examined do not correlate significantly with the emotional dimensions, except
for image brightness. There is a small tendency for positive images to be
slightly brighter than the average in the IAPS set. Not surprisingly, the effect
of increased brightness is to shift the scale of the performance curve in the
RSVP task, without affecting its shape. This is expected from the fact that
brighter images might elicit stronger and faster responses in the early filters,
thus increasing the amount of information made available per unit time. More
sophisticated analyses of low-level image statistics and their ability to
support an automatic classification of emotional content in scenes will be
discussed in a companion study (for a preliminary report, see Maljkovic et al.,
2004). Suffice to say here that we are
unaware of any statistical algorithm capable of mimicking the human in this
respect. It is after all not so surprising that low-level image properties
cannot separate the emotional categories: Unlike other categorization tasks, for
example, cityscapes versus landscapes (Torralba & Oliva, 2003; Vailaya, Jain, & Zhang, 1998), where same category exemplars share
substantial physical similarities, emotional categories contain material that is
very heterogeneous, and, therefore, very hard to classify based on statistical,
physical image properties.
In Experiment 2 we
have shown that observers are able to categorize the emotional content of scenes
with very brief exposures, already giving a better than chance performance with
only one video frame of exposure. Many recent (Keysers et al., 2001; Li et al., 2002; Thorpe et al., 1996; VanRullen & Thorpe, 2001a, 2001b) and older (Biederman, Rabinowitz,
Glass, & Stacy, 1974) studies have
shown that a very brief, masked presentation of visual stimuli is sufficient to
allow for a variety of categorization tasks. These observations have sparked a
lively debate concerning the nature of the underlying neural processing. In
contrast to popular accounts of object recognition attributing an essential role
to feedback activity from higher level centers (Mumford, 1991, 1992), the results of these experiments seem
more compatible with an essentially feed-forward mechanism (VanRullen &
Koch, 2003). While the categorization in
many previous studies, similar in spirit to our own, could be based on
differences in low-level image statistics (Johnson & Olshausen, 2003), such an explanation does not seem to
hold in our case, a point we return to below. Whichever the mechanistic basis of
such categorization ability, its temporal course is transient in nature: Most of
the information accrual necessary to perform the task happens in the first
≈200 ms after stimulus onset. This temporal pattern distinguishes the
categorization task from the RSVP task, which instead proves to depend on a
sustained accumulation of information over at least ≈2 s of exposure to
the stimulus. Furthermore, in the rating task, positive and negative images
display similar categorization dynamics, unlike in the RSVP task. Thus, an early
comprehension of the emotional content of the scene could allow for an
intelligent management of the limited resources of VSTM.
The matching-to-sample-task that we have used in
Experiment 3 does not require encoding in
short-term memory and has been used as a baseline comparison in many previous
studies of working memory (Gaffan, 1974).
Similarly, our aim was to obtain a baseline with which to compare the effects of
the RSVP task. We have found a total absence of a specific effect of valence on
performance in the matching task, which converges with the evidence discussed so
far in suggesting that negative valence exerts a specific effect only on
VSTM.
Differences in long-term memory encoding and retrieval
of emotional material are well documented: It is generally found that emotional
information is remembered better than neutral information (Hamann, 2001). Given that the average emotional charge
of negative images might have been higher than positive images in arousal and/or
in valence content, one may wonder whether long-term effects could have
contaminated our task and been responsible for the observed pattern of behavior.
Long-term influences can be studied in the RSVP task by examining the effect of
serial testing position (i.e., of the order in which each picture was shown
during the recognition stage). If there is memory leakage and other factors
being equal, pictures tested later in the recognition stage should be remembered
less than pictures tested earlier. A detailed analysis of long-term memory
effects in the RSVP task is beyond the scope of the present study and will be
presented in a separate paper. Suffice to say here that memory for positive
images, but not for negative images, shows a small leakage (≈10% across
all exposures). The critical question is whether this memory leakage can account
for the pattern of temporal dynamics we have uncovered in the RSVP task. The
analysis of performance with images shown early and late in the recognition
stage reveals that the shape of the psychometric functions does not change with
testing position. Thus, a selective long-term memory leakage does not seem to be
the source of the effects we have documented.
A variety of other accounts based on serial position
effects could also be entertained. We address here two accounts most commonly
discussed in RSVP studies. First is the possibility that performance with the
current image is better or worse when preceded by a negative image than a
positive one. We have analyzed the performance with neutral images when preceded
by negative or positive pictures and have found no evidence of serial
presentation position effects in this case. The second account is the possible
lack of “attentional blink” (AB) for negative stimuli. The
attentional blink refers to the finding that a second target is frequently
missed when it appears 200-500 ms after the onset of a first target. In a recent
study, it was demonstrated that negative words presented within an RSVP stream
do not suffer the AB (Anderson & Phelps, 2001). The present data are compatible with
the concept of a reduced AB for negative material inasmuch as performance with
negative images at exposures longer than ≈400 ms is at least as good or
better than with positive images. However, if this type of effect is to explain
the present data, then one should predict a stronger attentional blink for
negative than positive pictures at very short exposures (<100 ms), an effect
which would disappear or reverse after ≈250 ms. To our knowledge this
pattern has never been demonstrated. Thus no known serial position effects
account for the memory accumulation results we report here.
What then is the nature of the effects of valence on
VSTM? The storage function of VSTM is limited and slow to be deployed. Thus it
has the characteristics of a precious, limited capacity resource, which needs to
be carefully managed. Selection and management mechanisms need to be in place to
direct the appropriate deployment of such resource. One of the most widely
studied of such mechanisms is attention: It ensures that task-relevant stimuli
are processed better and faster at the expense of other, less relevant stimuli.
It is the motivational system, however, that understands the wider goals of the
organism in terms of approach and avoidance reactions. Thus it is reasonable to
assume that optimal behavior needs the integration of both systems, the
attentional and the emotional. Attention speeds up information accrual: This was
clearly demonstrated by Carrasco and colleagues (Carrasco & McElree, 2001), who showed that the time constant of
the exponential function describing accuracy of visual search as function of
display exposure is faster when the search array is preceded by an exogenous
informative cue. It is tempting to speculate that negative valence might act as
an endogenous attentional cue, thus
leading to a speed-up of information accrual similar in nature to that obtained
by exogenous cues. However, unlike Carrasco, who proposes that transient covert
attention increases the gain of early detectors (Carrasco, Ling, & Read, 2004), we envisage the effect of negative
valence as a later process, acting at the level of short-term memory storage.
The time-course of the effect we observe seems too slow to be compatible with a
classic gain control mechanism, and no evidence of such effect is observed in
tasks where short-term memory involvement is presumed to be minimal
( Experiments 2 and
3). Furthermore, the effect appears complex:
Recall that the hazard rate for negative images in the RSVP task not only
accelerates over time, but also starts from a lower level than for positive or
neutral images. Reluctant as we may be to put forward an explanation of such a
feature at this stage, it is possible that image features most diagnostic of
negative content attract most of the early processing resources at the expense
of the wider context, thus hindering recognition memory (conjectures of similar
kind have often been advanced in past studies and most recently by Kensinger
& Corkin, 2003). Thus, a more
appropriate metaphor for the effects of negative valence might be that of a
gating system, decreasing then increasing information flow to visual short-term
memory. From a teleological standpoint, neutral and positive images do not
represent a challenge to the organism, and information accrual from such sources
can be let to follow a free-flow, random sampling regime. Conversely, negative
images might represent a threat that requires a fast and costly reaction, thus
demanding a more accurate and controlled flow of
information.
This research was supported by National Institutes of
Health Grant R01-EY13155.
We wish to thank Hany Farid for consulting on image
statistics, Mari Sian Davies for piloting the memory experiment, and Julie
Berger for her invaluable contributions to all aspects of experimental design.
We thank the three anonymous reviewers for their very constructive criticism and
helpful suggestions. Commercial
relationships: none.
Corresponding author: Vera Maljkovic.
Email: v-maljkovic@uchicago.edu.
Address: 5848 S. University Ave., Chicago, IL 60637.
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