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The Journal of Neuroscience, January 1, 1998, 18(1):411-418
Masked Presentations of Emotional Facial Expressions Modulate
Amygdala Activity without Explicit Knowledge
Paul J.
Whalen,
Scott L.
Rauch,
Nancy L.
Etcoff,
Sean C.
McInerney,
Michael B.
Lee, and
Michael A.
Jenike
Psychiatric Neuroimaging Research Group and Nuclear Magnetic
Resonance Center, Massachusetts General Hospital and Harvard Medical
School, Boston, MA 02115
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ABSTRACT |
Functional magnetic resonance imaging (fMRI) of the human brain was
used to study whether the amygdala is activated in response to
emotional stimuli, even in the absence of explicit knowledge that such
stimuli were presented. Pictures of human faces bearing fearful or
happy expressions were presented to 10 normal, healthy subjects by
using a backward masking procedure that resulted in 8 of 10 subjects
reporting that they had not seen these facial expressions. The backward
masking procedure consisted of 33 msec presentations of fearful or
happy facial expressions, their offset coincident with the onset of 167 msec presentations of neutral facial expressions. Although subjects
reported seeing only neutral faces, blood oxygen level-dependent (BOLD)
fMRI signal in the amygdala was significantly higher during viewing of
masked fearful faces than during the viewing of masked happy faces.
This difference was composed of significant signal increases in the
amygdala to masked fearful faces as well as significant signal
decreases to masked happy faces, consistent with the notion that the
level of amygdala activation is affected differentially by the
emotional valence of external stimuli. In addition, these facial
expressions activated the sublenticular substantia innominata (SI),
where signal increases were observed to both fearful and happy
faces suggesting a spatial dissociation of territories that respond to
emotional valence versus salience or arousal value. This study, using
fMRI in conjunction with masked stimulus presentations, represents an
initial step toward determining the role of the amygdala in nonconscious processing.
Key words:
amygdala; extended amygdala; substantia innominata; nucleus basalis of Meynert; bed nucleus of the stria terminalis; emotion; facial expression; backward masking; awareness; fMRI; neuroimaging
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INTRODUCTION |
Neuroscientific research provides
many examples of tasks executed below the level of awareness (Schacter
et al., 1993 ; He et al., 1996; Berns et al., 1997; Rauch et al., 1997).
It has been argued that initial responses to affective stimuli are
automatic and do not require awareness (Zajonc, 1980). The amygdala is
a brain area located within the medial temporal lobe that is known to
process affective or emotionally valenced stimuli (see Aggleton, 1992).
On the basis, in part, of animal studies demonstrating a direct
short-latency pathway from the thalamus to the amygdala (LeDoux et al.,
1985), LeDoux (1996) has proposed that the amygdala might survey
emotionally valenced stimuli without awareness. Consistent with this
notion, studies of human subjects by Öhman and colleagues (Öhman, 1992) have demonstrated skin conductance responses to emotionally valenced facial expressions conditioned to predict an
aversive electrical shock when these expressions were presented in a
manner that prevented awareness (i.e., backward masking). Taking a lead
from human lesion data (Adolphs et al., 1995; Calder et al., 1996),
recent neuroimaging reports in humans have demonstrated activation
within the amygdala in response to facial expressions of emotion
(Breiter et al., 1996; Morris et al., 1996). The present study used
functional magnetic resonance imaging (fMRI) during the presentation of
backwardly masked facial expressions to determine whether amygdala
activation might be demonstrated in humans in the absence of explicit
knowledge.
A backward masking procedure previously demonstrated to interrupt
processing of emotionally expressive faces (Esteves and Öhman,
1993; Rolls and Tovee, 1994) was used. Each masked stimulus consisted
of a 33 msec fearful or happy expression face (target), its offset
coincident with the onset of a 167 msec neutral expression face (mask).
Esteves and Öhman (1993) demonstrated that if the stimulus onset
asynchrony (SOA; i.e., the interval between the onset of the target and
the mask) was sufficiently brief (<40 msec), human subjects were not
aware of the emotionally expressive target face, as defined by
objective forced choice tasks and subjective report. In the present
study 10 human subjects viewed repeating 28 sec epochs that consisted
of either fearful faces masked by neutral faces, happy faces masked by
neutral faces, or a single cross (+) that served as a fixation point
baseline. We predicted that, although subjects would report seeing only
the neutral masks, blood oxygen level-dependent (BOLD) fMRI signal
intensity (Kwong et al., 1992; Ogawa et al., 1992) would increase in
the amygdala in response to masked fearful targets when compared with
masked happy targets. In addition, we predicted that presentation of masked emotional facial expressions would serve to isolate amygdala activation in contrast to previous neuroimaging studies of nonmasked facial expressions, which have demonstrated activation of the amygdala
along with numerous additional brain regions (Breiter et al., 1996;
Morris et al., 1996).
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MATERIALS AND METHODS |
Subjects. Ten right-handed males aged 19-32 (mean,
23.8 years) provided informed consent before participation in this
study, according to guidelines established by the Subcommittee on Human Studies at the Massachusetts General Hospital. Handedness was defined
by the Edinburgh Inventory (Oldfield, 1971). Subjects were told that
they would be presented with pictures of faces. All subjects were naive
to the face stimuli used and to our hypotheses pertaining to the
emotional expressions of faces. For this initial experiment a single
gender cohort was studied to minimize heterogeneity, thereby improving
statistical power. Future studies of female subjects will be necessary
to determine the generalizability of the current results.
Selection of fear faces as threat-related stimuli. Face
stimuli consisted of fearful, happy, and neutral expressions of eight individuals (numbers 021, 030, 040, 081, 101, 121, 131, 140; Ekman and
Friesen, 1976). We selected fearful faces as our negatively valenced
stimuli because human lesion studies document a deficit in the
processing of fearful faces after amygdala lesions (Adolphs et al.,
1995; Calder et al., 1996), and previous neuroimaging studies
demonstrate amygdala activation to these stimuli (Breiter et al., 1996;
Morris et al., 1996). We offer the concept that, unlike an angry face
that represents a direct threat, the relationship of a fearful face to
threat is ambiguous in that a fearful face signals the presence of
danger, but not its source. In this sense, a fearful face can be
conceptualized as a contextual stimulus, whereas an angry face can be
conceptualized as a specific cue.
Paradigm. Subjects were presented with alternating 28 sec
epochs of masked fearful face targets (F), masked happy face targets (H), or a single cross that served as a low-level fixation condition (+). During each epoch subjects viewed either 56 masked fearful stimuli
or 56 masked happy stimuli (each of eight fearful or happy faces was
masked by the neutral expression for each of the other seven
individuals).
Masked stimuli were presented twice per second in a random order. Each
200 msec masked stimulus consisted of a 33 msec fearful or happy
expression (target) immediately followed by a 167 msec neutral
expression (mask).
The order of 28 sec epochs containing 56 fearful or happy masked
stimuli was counterbalanced within and across subjects; one-half of the
subjects viewed masked fearful, followed by masked happy, targets
during their first run (+,F,H,+,F,H,+,F,H,+); the other half viewed
masked happy, followed by masked fearful, targets during their first
run (+,H,F,+,H,F,+,H,F,+). Then the order of fearful and happy target
epochs was reversed for the second run for all subjects. These 10 epochs comprised a 4 min and 40 sec run. Each subject viewed two
runs.
Subject debriefing. Subjective report measures were used to
assess the subjects' explicit knowledge of presented masked facial expressions of emotion after the completion of all stimulus
presentations. Immediately after the experiment the subjects were asked
to describe any aspect of the presented faces. Next, the subjects were
asked to comment on the emotional expressions of the faces. Then the subjects were asked if they had seen any happy or smiling faces and
asked if they had seen any fearful or afraid faces. Finally, the
subjects were shown all face stimuli (fearful, happy, and neutral) and
asked to point out the specific faces they had referred to in response
to earlier questions.
Stimuli and apparatus. Face stimuli consisted of PICT files
that were assembled frame by frame into a film, using Adobe Premiere software. Specialized hardware (Media 100, Marlboro, MA) was used to
transfer the digital PICT information to videotape synchronized with
the headsweeps of the VCR so as not to distort the stimuli. A VCR was
used to play the tape, and the output was projected (Sharp XG-2000U
LCD) onto a screen within the imaging chamber, viewable by a mirror
(1.5 × 3.5 inches) ~6.5 inches from the subject's face. The
play speed of the VCR was 30 frames/sec, creating a 33 msec/frame
presentation rate.
Pulse rate was measured from the right index finger of all subjects
during stimulus presentations via pulse oximetry (In Vivo Systems,
Orlando, FL).
Functional magnetic resonance images were collected in a General
Electric Signa 1.5 Tesla high-speed imaging device (modified by
Advanced NMR Systems, Wilmington, MA), using a quadrature head coil.
Our Instascan software is a variant of the echo planar technique first
described by Mansfield (1977). Head stabilization was achieved with a
plastic bite bar molded to each subject's dentition.
Image acquisition and data analysis. Our standard image
acquisition protocol was used and previously has been detailed
elsewhere (Cohen and Weisskoff, 1991; Kwong, 1995). An initial sagittal localizer [spoiled gradient recall acquisition in a steady state (SPGR), 60 slices, resolution 0.898 × 0.898 × 2.8 mm] was
performed to provide a reference for future slice selection and for
eventual localization within Talairach space (Talairach and Tournoux,
1988). After automated shimming (Reese et al., 1995) to maximize field homogeneity, a magnetic resonance (MR) angiogram (SPGR, resolution 0.78125 × 0.78125 × 2.8 mm) was acquired to identify large-
and medium-diameter vessels. Then a set of T1-weighted high-resolution transaxial anatomic scans (resolution 3.125 × 3.125 × 8 mm)
was acquired. For the functional series, asymmetric spin echo (ASE) sequences were used to minimize macrovascular signal contributions. Functional ASE data were acquired as 15 contiguous, interleaved, horizontal 8 mm slices that paralleled the intercommissural plane (voxel size 3.125 × 3.125 × 8 mm; 100 images per slice,
TR/TE/Flip = 2800 msec/70 msec/90°).
Automated data analytic techniques began with a quantification of
subject motion and then correction, using an algorithm developed by
Jiang et al. (1995), based on Woods et al. (1992). Both functional and
high-resolution structural data were placed into normalized Talairach
space and resliced into 3.125 × 3.125 × 3 mm voxels in the
coronal plane. Then data from individuals were baseline-normalized and
concatenated (averaged). Nonparametric statistical maps were calculated
with the Kolmogorov-Smirnov (KS) statistic, displayed in pseudocolor,
scaled according to significance, and superimposed on T1-weighted
high-resolution images also placed into Talairach space and resliced in
the coronal plane. Because we predicted only amygdala activation to the
present experimental manipulation, our a priori significance threshold
(p < 6.6 × 10 4)
represents a Bonferroni-corrected 0.05 probability level based on the
~76 voxels that make up the amygdaloid region (Filipek et al.,
1994).
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RESULTS |
Subject debriefing
Immediately after the experiment, the subjects were asked to
describe any aspect of the presented faces. Two of the 10 subjects offered descriptions indicating that they had seen features of the
emotional target stimuli. The remaining eight subjects were asked next
to comment on the emotional expressions of the faces, and all responded
with reference to the neutral mask stimuli alone. Then the subjects
were asked if they had seen any happy or fearful faces. All eight
subjects reported that they had not seen these expressions. Finally,
these eight subjects were shown all face stimuli (fearful, happy, and
neutral) and asked to point out the specific faces they had seen.
Subjects selected only neutral faces. Therefore, we present here brain
activation data for the eight subjects who reported having seen only
the neutral faces.
Pulse rate data
Pulse rate was measured in the eight subjects who reported not
having seen the masked fearful and happy faces (sampled approximately every 5 sec). Technical problems prevented measurement within the
magnet for two of these subjects. Results revealed no significant pulse
rate changes to the presentation of fearful or happy faces when
compared with one another or the fixation baseline condition (p > 0.05).
fMRI data
Figure 1 presents BOLD signal
changes across whole brain in response to masked fearful faces versus
masked happy faces for the eight subjects who demonstrated no explicit
knowledge of the presence of these stimuli. Note the relative absence
of activation outside the amygdaloid region.
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Figure 1.
Masked fearful faces versus masked happy faces.
Areas of significant activation (p < 6.6 × 104) across whole brain, presented
here as 57, 3 mm coronal slices for the masked fear versus masked happy
contrast, for the eight subjects who reported not having seen the
fearful or happy target faces. All figures are displayed according to
radiological convention (i.e., left = right; right = left;
top = superior; bottom = inferior). The most anterior slice
is in the top left corner, and slices proceed in a
posterior direction from left to right
and then down. The colorized statistical map is
superimposed over the averaged high-resolution structural data for
these eight subjects. Both functional and structural data have been
placed in a normalized space according to the coordinate system of
Talairach and Tournoux (1988). All figures were smoothed by using a
Hamming nine voxel 1:2:1 kernel filter, although activations were
significant on unsmoothed maps. Significant activation within the
amygdaloid region is evident within two slices in the third row
(yellow brackets). These two slices represent
Talairach coordinates in the y-plane of 0 (see Fig. 3)
and  6 (see Fig. 2), respectively. Note also the relative lack of
activation across all other brain regions. There is an activation of
the inferior prefrontal cortex (first row, slice nine) that met the
significance level set a priori for the amygdala. Note that, although
our 15 original horizontal slice acquisitions covered "whole
brain," susceptibility from the sinus space causes signal dropout in
portions of some brain regions (see Results).
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Figure 2A presents the
most posterior coronal slice from the amygdaloid region of activation
depicted in Figure 1. Significantly higher BOLD signal is observed in
the amygdala in response to masked fearful faces (467.56 ± 0.41, mean ± SEM) when compared with masked happy faces (464.85 ± 0.43, mean ± SEM). Four contiguous voxels within the right
amygdala met the threshold for statistical significance
(p < 6.6 × 10 4; see
Materials and Methods). We then assessed the direction of signal change
to fearful or happy faces in comparison to the fixation baseline
epochs. We considered only the four significantly activated voxels from
the fear versus happy contrast depicted in Figure 2A;
the masked fear versus fixation contrast revealed a significant increase in signal intensity, whereas the masked happy versus fixation
contrast revealed a significant decrease in signal intensity. For this
comparison we treated the four voxels in the amygdala (defined by the
overall fear vs happy contrast) as one region of interest (ROI). Mean
signal intensity within this ROI demonstrated a significant increase to
masked fearful faces and a significant decrease to masked happy faces
when compared with fixation (p < 0.05). Thus,
the larger overall fear versus happy statistical effect
(p < 6.6 × 104)
demonstrated across these four voxels depends on both a response to the
fearful faces (increase) and the happy faces (decrease). By considering
only voxels activated in the fear versus happy contrast, we are assured
of describing only the nature of signal changes specifically
attributable to the emotional expressions.
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Figure 2.
Top. Amygdala activation to masked
fearful versus masked happy faces. A, Coronal display of
the most posterior slice depicting activation within the region of the
amygdala from Figure 1. Image parameters are as in Figure 1. Activation
depicted here in the right amygdala includes four contiguous voxels
that significantly increased in response to masked fearful faces when
compared with masked happy faces (p < 6.6 × 104). B, Bar graph
depicting changes in BOLD signal intensity as a function of repeated
stimulus presentations. Bars represent the mean
percentage change of signal intensity per epoch in response to masked
fearful and masked happy faces (counterbalanced), as compared with the
preceding and following low-level fixation conditions. Values reflect
only the four voxels that exceeded the Bonferroni-corrected significance threshold (depicted within A) for the
masked fearful versus masked happy contrast.
Figure 3.
Bottom. Amygdala/SI activation to masked
fearful versus masked happy faces. A, Coronal display of
the most anterior slice depicting activation within the region of the
amygdala from Figure 1. Image parameters are as in Figure 1. Note that
the most ventral portion of this activation is within the temporal lobe (where the most anterior extent of the amygdala is located). This activation then extends dorsally into the basal forebrain where the
sublenticular substantia innominata (SI) is
located. Six voxels met the Bonferroni-corrected significance threshold
(p < 6.6 × 104).
B, Enlargement of the activation presented in
A is presented twice: once for masked fear versus
fixation and again for masked happy versus fixation. Colors of enlarged
voxels represent significance levels for the original masked fear
versus masked happy contrast as follows: orange,
p < 6.6 × 104;
red, p < 0.005;
blue, p < 0.05. Although the
significant statistical effect for the masked fear versus masked happy
contrast in the ventral portion of this activation
(amyg) is attributable to signal increases to fearful
faces and signal decreases to happy faces (similar to the amygdala
activation in Fig. 2), the statistical effect in the dorsal portion of
this activation (SI) is a result of signal
increases to both fearful and happy faces in which increases to fearful
faces are significantly larger (p < 6.6 × 104).
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To delineate the effect of repeated presentations of these stimuli,
Figure 2B presents BOLD signal changes in the
amygdala for the significant ROI depicted in Figure
2A across all epochs of presentation. First, notice
that BOLD signal in the amygdala is always higher during presentation
of masked fear faces when compared with the contiguous
(counterbalanced) epoch of masked happy faces. For this group of eight
subjects the average percentage of change in signal intensity between
conditions (masked fear vs masked happy) ranged from 0.77 to 0.35%
across epochs. When compared with the fixation baseline condition,
signal intensity increases in response to fearful faces occurred during
the first two fear presentation epochs but were attenuated to baseline
with subsequent stimulus presentations. In contrast, however, note that
signal intensity decreases in response to happy faces persisted through
all presentation epochs.
Figure 3A depicts BOLD fMRI
signal changes for the masked fear versus happy contrast in the most
anterior coronal slice from the amygdaloid region of activation
depicted in Figure 1. The ventral portion of this activation is within
the temporal lobe, where the most anterior extent of the amygdala is
located; however, this activation extends immediately rostral and
dorsal to the traditionally defined amygdala within the region of the
sublenticular substantia innominata (SI) of the basal forebrain (see
Heimer et al., 1997). Within the SI this activation extends in a
dorsomedial direction to the base of the anterior commissure.
Although BOLD signal changes in the ventral portion of this activation
increased to fearful faces and decreased to happy faces (similar to the
activation in Fig. 2), significant BOLD signal changes in the dorsal
portion of this activation for the masked fear versus masked happy
contrast (p < 6.6 × 104) were created by signal increases to
both fearful and happy faces, in which increases to fearful
faces were significantly larger. Figure 3B presents an
enlargement of the significant voxels of activation from the masked
fear versus masked happy contrast pictured in Figure 3A. The
activation is presented twice: once for the fear versus fixation
contrast and again for the happy versus fixation contrast. Numbers
overlying the voxels present the average percentage of BOLD signal
change from the fixation baseline across all stimulus presentations.
Note that, in response to masked fear faces, all voxels of
activationthe most ventral voxels located in the amygdala and the
most dorsal voxels located in the SIdemonstrate signal increases. In
contrast, in response to masked happy faces, ventrally located voxels
demonstrate signal decreases (similar to the amygdala response depicted
in Fig. 2), whereas dorsal voxels located in the SI demonstrate signal
increases.
Table 1 presents Talairach coordinates
(Talairach and Tournoux, 1988) and probability values of activated
brain regions for the masked fear versus happy contrast for the eight
subjects that reported not having seen the masked fearful and happy
faces. Activation within the left and right amygdala exceeded the a
priori threshold for significant activation (p < 6.6 × 104). To obviate bias, we report
here all areas of activation across whole brain that met this
threshold. One other brain area, left inferior prefrontal cortex, also
met this criterion (see Fig. 1, row one, slice nine). Because it was
not predicted, we note then that activation in this region did not
achieve the appropriate Bonferroni-corrected threshold for whole brain
(p < 1.0 × 107).
Technical considerations
Quantification of motionCorrected motion during functional image
acquisition was <1.5 mm for all subjects. Missing dataA computer
failure during image acquisition of subject number 7 caused his first
run to be lost. This did not affect the results, because statistical
effects were similar whether six, seven, or eight subjects were
considered. The fact that the results were similar to those of six
subjects is important, because loss of these data did not compromise
the protection afforded by counterbalancing. Vessel effectsTo rule
out the possibility that the observed activations were attributable to
flow through large vessels located medial to the temporal lobe (e.g.,
inferior carotid, middle cerebral artery), we acquired MR angiograms
for these eight subjects, placed them into normalized Talairach space,
and then averaged them across the subjects. Thus, the composite
activations for eight subjects did not overlie the location of large
vessels on averaged MR angiograms. Susceptibility artifactIt is
unlikely that the observed activation is an artifact of changes in the
nearby field of susceptibility because (1) inspection of animated raw
signal intensity changes over time revealed no obvious systematic
changes in susceptibility that mirrored counterbalanced conditions, and
(2) these results (i.e., increased signal to fear, decreased signal to
happy) are consistent with a previous positron emission tomography
(PET) study using nonmasked stimuli, where susceptibility is not a
concern.
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DISCUSSION |
Significance of amygdala activation to masked stimuli
Amygdala activation was observed in response to masked fearful
faces versus masked happy target faces that subjects reported not
having seen. As predicted, the backward masking of emotional facial
expressions resulted in impressive isolation of the amygdala. This
finding is particularly striking when considered in light of an earlier
neuroimaging study demonstrating activation of the amygdala and four
additional brain regions to presentation of nonmasked fearful faces
versus happy faces (Morris et al., 1996).
These data highlight the automaticity of the amygdala response and are
consistent with the assertion of LeDoux (1996) that the amygdala
responds to early, crude representations of external stimuli. Although
consistent with the notion that the amygdala might receive stimulus
information directly from the thalamus (LeDoux et al., 1985), prior or
parallel to elaborate cortical processing, the temporal resolution of
the present design (based on 28 sec epoch lengths) does not address
this issue directly. In addition, portions of candidate cortical areas
that also might survey masked facial stimuli [e.g., temporal visual
cortex (Hasselmo et al., 1989) and ventral prefrontal cortex (Tranel et
al., 1995; Hornak et al., 1996)] may not have been visualized in the
present study because of characteristic signal drop-out associated with fMRI caused by the nearby sinus space. Replication of the present effect using PET (where susceptibility drop-out is not an issue) would
address this concern.
Direction of signal changes in the amygdala
Within the amygdala, signal intensity increased to masked fear
faces and decreased to masked happy faces, consistent with a previous
imaging study (Morris et al., 1996). In addition, signal increases to
masked fearful faces habituated. Habituation of response within the
amygdala to emotionally valenced stimuli that have proven
inconsequential is consistent with previous reports in both animals
(Bordi et al., 1993) and humans (Breiter et al., 1996; Irwin et al.,
1996). In contrast, however, signal intensity decreases in response to
happy faces persisted through all presentation epochs. Happy faces
appear to provide information of enduring importance and, in this
sense, might be conceptualized as safety signals. One interpretation of
these data is that both fearful and happy faces provide information
about the potential for threat in a given environment, differentially
affecting the level of activity in the amygdala.
This differential amygdala response, based on the valence of facial
expressions, is consistent with a recent study of human infants in
which presentation of negatively valenced (angry) faces produced
increased eyeblink magnitudes and positively valenced (happy) faces
produced decreased eyeblink magnitudes [Balaban (1995); see also Lang
(1995)]. Activation of the amygdala is known to modulate eyeblink
reflex sensitivity (Davis, 1992). To elaborate, although direct
electrical stimulation of the amygdala in animals does not produce an
eyeblink, the magnitude of the next eyeblink that is elicited after
amygdala stimulation is modified (Whalen and Kapp, 1991). These
converging results imply that, although amygdala activation to
experimental presentation of emotionally valenced facial expressions
may not produce obvious overt responses, it modifies overt responses to
subsequent sensory information through numerous efferent
pathways (see Kapp et al., 1992).
Significance of SI activation
The present experiment also produced activation that extended into
the sublenticular SI of the basal forebrain, consistent with recent PET
studies demonstrating blood flow changes within the SI that correlate
with (1) recall of negatively valenced film stimuli (Cahill et al.,
1996) as well as (2) thalamic responses to aversively conditioned
stimuli (Morris et al., 1997). These data are also consistent with an
emerging understanding of the inter-related anatomy of this region. For
example, the "extended amygdala," including the bed nucleus of the
stria terminalis (BNST; see Davis et al., 1997), describes a subset of
neurons within the SI characterized as a functional and anatomical
continuum of the traditionally defined amygdala, based on similarities
in cytoarchitecture as well as neurotransmitter and projection systems (Heimer et al., 1997). In addition, the amygdala is known to project directly to the SI (Russchen et al., 1985) where the cholinergic nucleus basalis of Meynert (NBM) neurons are located (Mesulam et al.,
1983).
The present demonstration of increased activation of the SI to
both fearful and happy faces is consistent with (1) data in primates demonstrating increased neuronal responses in the SI to both
positive (Richardson et al., 1988; Wilson and Rolls, 1990) and negative
(Whalen et al., 1994) stimuli, (2) the well established role of the NBM
in the modulation of cortical neuronal excitability (Celesia and
Jasper, 1966; Szerb, 1967; Sillitto and Kemp, 1983; Metherate and Ashe,
1991), and (3) the fact that the activity of these neurons is more
closely associated with an animal's overall state of vigilance or
arousal rather than with its response to specific stimulus
presentations (Detari and Vanderwolf, 1987; Whalen et al., 1994). Thus,
activation of the SI to both fearful and happy facial expressions might
represent a more generalized response to the salience (see Morris et
al., 1997) or arousal value (see Kapp et al., 1992; Whalen et al.,
1994) of these stimuli.
The dissociation between an amygdala response based on valence and an
SI response based on arousal offers a possible neuroanatomical substrate for psychophysiological responses long hypothesized by Lang
and colleagues to reflect emotional "action dispositions," based on
the valence versus arousal value of presented stimuli (see Lang, 1995;
Shupp et al., 1997). In addition, this response dissociation replicates
both the earlier Morris et al. (1996) and Breiter et al. (1996)
findings and clarifies response differences between the two studies. To
elaborate, in the present study the amygdala demonstrated increases to
fear and decreases to happy faces, similar to Morris et al. (1996);
activations that extended into the SI demonstrated increases to both
fear and happy faces, similar to Breiter et al. (1996).
Explicit knowledge and the determination of awareness
The present study was designed as a demonstration of the
automaticity of amygdala response and as an initial effort toward determining whether awareness is a prerequisite for amygdala
activation. Toward this end we used a stimulus onset asynchrony (SOA)
parameter (33 msec) below a threshold previously determined to prevent
awareness of masked emotional facial expressions (Esteves and
Öhman, 1993). Still, numerous methodological differences between
the present and previous studies preclude generalizations about
awareness on the basis of the parameter of SOA alone.
There are several challenges associated with the measurement of
awareness (see Merikle, 1992; Greenwald et al., 1996). These include
the timing of measurement [during interstimulus intervals (ISIs) vs after completion of all stimulus presentations] and the
type of measurement (objective vs subjective; recall vs
recognition). For this initial study we chose to assess awareness
subjectively after completion of all stimulus presentations,
emphasizing recall versus recognition measures. The timing we chose
does limit interpretation, to the extent that debriefing results may
not accurately reflect the subjects' awareness at the time of
presentation. However, this strategy (1) allowed for shorter ISIs,
maximizing the number of masked facial expressions presented within
each epoch and thereby protecting against type II error in terms of
amygdala activation, and (2) obviated the need for subjects to be
informed of the presence of masked stimuli before the study so that
findings would not be confounded by explicit attempts to detect
emotional expressions. Our reliance on recall versus recognition
measures of explicit knowledge was guided by research demonstrating
that recognition tasks requiring discrimination of very similar stimuli
are more susceptible to incorrect identification of target items
(Underwood, 1965; Roediger, 1980; Hintzman et al., 1992; Hintzman and
Curran, 1995; Mäntylä, 1997). With specific reference to
face stimuli, Mäntylä has demonstrated that recognition of
faces is driven by familiarity processes versus detailed episodic
information (Mäntylä, 1997).
An interstimulus objective forced choice task remains the "gold
standard" for the definition of awareness in behavioral psychology (see Greenwald et al., 1996). Future studies using such an
interstimulus measure would address the question of awareness directly
but would change the nature of the task fundamentally (active search vs passive viewing). Use of an objective forced choice measure after completion of all stimulus presentations may enable the objective assessment of awareness during a passive viewing task, although this
approach assumes that only consciously perceived information will
influence objective responses (see Jacoby, 1991; Merikle, 1992; Seamon
et al., 1995).
Conclusions and future direction
The role of the amygdala in fear conditioning is well established
(Aggleton, 1992), and the more recent reports of its involvement in the
processing of emotional facial expression (Adolphs et al., 1995;
Breiter et al., 1996; Calder et al., 1996; Morris et al., 1996) are
consistent with this role. The present study builds on the growing
number of neuroimaging studies demonstrating that human amygdala
activation in response to emotionally valenced stimuli is a reliable
phenomenon (Breiter et al., 1996; Cahill et al., 1996; Irwin et al.,
1996; Morris et al., 1996; Reiman et al., 1997). Specifically, we
demonstrated isolated amygdala activation in response to masked
presentations of facial expressions that prevented explicit knowledge.
These data underscore the automaticity (see McNally, 1995) of the
processing of the emotional facial expressions of the amygdala and are
consistent with data implicating the amygdala in the nonconscious
monitoring of emotional stimuli (Halgren, 1992; Öhman, 1992;
LeDoux, 1996).
In light of the present findings, we note that subjects with anxiety
disorders demonstrate (1) amygdala activation in association with
symptoms (see Rauch and Shin, 1997) and (2) information-processing biases during nonconscious processing (see Öhman, 1992; Mathews and MacLeod, 1994; Mogg et al., 1995; McNally et al., 1996). We are
developing fMRI probes, using masked stimulus presentations, in an
attempt to elucidate the role of the amygdala in the clinical phenomena
observed across the anxiety disorders (e.g., hypervigilance, failure to
habituate, exaggerated startle, etc.).
| |
FOOTNOTES |
Received Aug. 28, 1997; revised Oct. 13, 1997; accepted Oct. 20, 1997.
This work was supported by a Harvard Medical School Clinical Research
Training Program (CRTP) Fellowship to P.J.W. (MH-16259; Robert McCarley
and Stuart Hauser, Program Directors), MH-01215 and National Alliance
for Research on Schizophrenia and Depression Award to S.L.R., and the
David A. Judah Fund to M.A.J. We thank Terry Campbell, Mary Foley, Ivan
Audouin, Sherry Pai, Aiping Jiang, and George Bush for technical
assistance; and Richard McNally, Bruce Kapp, Tim Curran, Daniel
Schacter, Robert Savoy, Randy Buckner, Cary Savage, Elizabeth Phelps,
and Bruce Rosen for advice and comments.
Correspondence should be addressed to Dr. Paul J. Whalen, Department of
Psychiatry, Massachusetts General Hospital, 13th Street, Building 149, CNY-9, Charlestown, MA 02129. E-mail: paulw{at}nmr.mgh.harvard.edu
| |
REFERENCES |
-
Adolphs R,
Tranel D,
Damasio H,
Damasio A
(1995)
Fear and the human amygdala.
J Neurosci
15:5879-5891[Abstract].
-
Aggleton JP
editors
(1992)
In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley.
-
Balaban MT
(1995)
Affective influences on startle in five month old infants: reactions to facial expressions of emotion.
Child Dev
66:28-36[Web of Science][Medline].
-
Berns GS,
Cohen JD,
Mintun MA
(1997)
Brain regions responsive to novelty in the absence of awareness.
Science
276:1272-1275[Abstract/Free Full Text].
-
Bordi F,
LeDoux JE,
Clugnet MC,
Pavlides C
(1993)
Single-unit activity in the lateral nucleus of the amygdala and overlying areas of striatum in freely behaving rats: rates, discharge patterns, and responses to acoustic stimuli.
Behav Neurosci
107:757-769[Web of Science][Medline].
-
Breiter HC,
Etcoff NL,
Whalen PJ,
Kennedy WA,
Rauch SL,
Buckner RL,
Strauss MM,
Hyman SE,
Rosen BR
(1996)
Response and habituation of the human amygdala during visual processing of facial expression.
Neuron
17:875-887[Web of Science][Medline].
-
Cahill L,
Haier RJ,
Fallon J,
Alkire MT,
Tang C,
Keator D,
Wu J,
McGaugh JL
(1996)
Amygdala activity at encoding correlated with long-term, free recall of emotional information.
Proc Natl Acad Sci USA
93:8016-8021[Abstract/Free Full Text].
-
Calder AJ,
Young AW,
Rowland D,
Perrett DI,
Hodges JR,
Etcoff NL
(1996)
Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear.
Cognit Neuropsychol
13:699-745.
-
Celesia GG,
Jasper HH
(1966)
Acetylcholine released from cerebral cortex in relation to state of activation.
Neurology
16:1053-1064[Free Full Text].
-
Cohen MS,
Weisskoff RM
(1991)
Ultra-fast imaging.
Magn Reson Imaging
9:1-37[Web of Science][Medline].
-
Davis M
(1992)
The role of the amygdala in conditioned fear.
In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction (Aggleton JP,
ed), pp 255-306. New York: Wiley.
-
Davis M,
Walker DL,
Lee Y
(1997)
Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex.
In: Psychobiology of posttraumatic stress disorder (Yehuda R,
McFarlane AC,
eds), pp 305-331. New York: New York Academy of Sciences.
-
DeArmond SJ,
Fusco MM,
Dewey MM
(1993)
In: Structure of the human brain, 3rd Ed, pp 140-141. New York: Oxford UP.
-
Detari L,
Vanderwolf CH
(1987)
Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anesthetized rats.
Brain Res
437:1-8[Web of Science][Medline].
-
Ekman P,
Friesen WV
(1976)
In: Pictures of facial affect. Palo Alto, CA: Consulting Psychologists.
-
Esteves F,
Öhman A
(1993)
Masking the face: recognition of emotional facial expressions as a function of the parameters of backward masking.
Scand J Psychol
34:1-18[Web of Science][Medline].
-
Filipek P,
Richelme C,
Kennedy D,
Caviness V
(1994)
The young adult human brain: an MRI-based morphometric analysis.
Cereb Cortex
4:344-360[Abstract/Free Full Text].
-
Greenwald AG,
Draine SC,
Abrams RL
(1996)
Three cognitive markers of unconscious semantic activation.
Science
273:1699-1702[Abstract/Free Full Text].
-
Halgren E
(1992)
Emotional neurophysiology of the human amygdala within the context of human cognition.
In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction (Aggleton JP,
ed), pp 191-228. New York: Wiley.
-
Hasselmo ME,
Rolls ET,
Baylis GC
(1989)
The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey.
Behav Brain Res
32:203-218[Web of Science][Medline].
-
He S,
Cavanaugh P,
Intrilligator J
(1996)
Attentional resolution and locus of visual awareness.
Nature
383:334-337[Medline].
-
Heimer L,
Harlan RE,
Alheid GF,
Garcia MM,
De Olmos J
(1997)
Substantia innominata: a notion which impedes clinical-anatomical correlations in neuropsychiatric disorders.
Neuroscience
76:957-1006[Web of Science][Medline].
-
Hintzman DL,
Curran T
(1995)
When encoding fails: instructions, feedback, and registration without learning.
Mem Cognit
23:213-226[Web of Science][Medline].
-
Hintzman DL,
Curran T,
Oppy B
(1992)
Effects of similarity and repetition on memory: registration without learning?
J Exp Psychol
18:667-680.
-
Hornak J,
Rolls ET,
Wade D
(1996)
Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage.
Neuropsychologia
34:247-261[Web of Science][Medline].
-
Irwin W,
Davidson RJ,
Lowe MJ,
Mock BJ,
Sorenson JA,
Turski PA
(1996)
Human amygdala activation detected with echo-planar functional magnetic resonance imaging.
NeuroReport
7:1765-1769[Web of Science][Medline].
-
Jacoby LL
(1991)
A process dissociation framework: separating automatic from intentional uses of memory.
J Mem Language
30:513-541.
-
Jiang A,
Kennedy DN,
Baker JR,
Weiskoff RM,
Tootell RBH,
Woods RP,
Benson RR,
Kwong KK,
Brady TJ,
Rosen BR,
Belliveau JW
(1995)
Motion detection and correction in functional MR imaging.
Hum Brain Mapp
3:224-235. [Web of Science]
-
Kapp BS,
Whalen PJ,
Supple WF,
Pascoe J
(1992)
Amygdaloid contributions to conditioned arousal and sensory information processing.
In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction (Aggleton JP,
ed), pp 229-254. New York: Wiley.
-
Kwong KK
(1995)
Functional magnetic resonance imaging with echo planar imaging.
Magn Reson Q
11:1-20[Web of Science][Medline].
-
Kwong KK,
Belliveau JW,
Chesler DA,
Goldberg IE,
Weisskoff RM,
Poncelet BP,
Kennedy DN,
Hoppel BE,
Cohen MS,
Turner R,
Cheng HM,
Brady TJ,
Rosen BR
(1992)
Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation.
Proc Natl Acad Sci USA
89:5675-5679[Abstract/Free Full Text].
-
Lang PJ
(1995)
The emotion probe: studies of motivation and attention.
Am Psychologist
50:372-385[Medline].
-
LeDoux JE
(1996)
In: The emotional brain. New York: Simon and Shuster.
-
LeDoux JE,
Ruggiero DA,
Reis DJ
(1985)
Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat.
J Comp Neurol
242:182-213[Web of Science][Medline].
-
Mansfield P
(1977)
Multi-planar image formation using NMR spin echoes.
J Physics [Suppl C]
10:L55-L58.
-
Mäntylä T
(1997)
Recollection of faces: remembering differences and knowing similarities.
J Exp Psychol
23:1203-1216.
-
Mathews A,
MacLeod C
(1994)
Cognitive approaches to emotion and emotional disorders.
Annu Rev Psychol
45:25-50[Web of Science][Medline].
-
McNally RJ
(1995)
Automaticity and the anxiety disorders.
Behav Res Ther
33:747-754[Web of Science][Medline].
-
McNally RJ,
Amir N,
Lipke HJ
(1996)
Subliminal processing of threat cues in posttraumatic stress disorder?
J Anxiety Disord
10:115-128.
-
Merikle PM
(1992)
Perception without awareness: critical issues.
Am Psychologist
47:792-796[Medline].
-
Mesulam M-M,
Mufson EI,
Wainer BH,
Levey AI
(1983)
Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6).
Neuroscience
10:1185-1201[Web of Science][Medline].
-
Metherate R,
Ashe JH
(1991)
Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors.
Brain Res
559:163-167[Web of Science][Medline].
-
Mogg K,
Bradley BP,
Williams R
(1995)
Attentional bias in anxiety and depression: the role of awareness.
Br J Clin Psychol
34:17-36.
-
Morris JS,
Frith CD,
Perrett DI,
Rowland D,
Young AW,
Calder AJ,
Dolan RJ
(1996)
A differential neural response in the human amygdala to fearful and happy facial expressions.
Nature
383:812-815[Medline].
-
Morris JS,
Friston KJ,
Dolan RJ
(1997)
Neural responses to salient visual stimuli.
Proc R Soc Lond [Biol]
264:769-775[Medline].
-
Ogawa S,
Tank DW,
Menon R,
Ellermann JM,
Kim SG,
Merkle H,
Ugurbil K
(1992)
Intrinsic signal changes accompanying sensory stimulation: functional brain mapping using MRI.
Proc Natl Acad Sci USA
89:5951-5955[Abstract/Free Full Text].
-
Öhman A
(1992)
Fear and anxiety as emotional phenomena: clinical phenomenology, evolutionary perspectives, and information-processing mechanisms.
In: Handbook of emotions (Lewis M,
Haviland JM,
eds), pp 511-536. New York: Guilford.
-
Oldfield RC
(1971)
The assessment and analysis of handedness: the Edinburgh inventory.
Neuropsychologia
9:97-113[Web of Science][Medline].
-
Rauch SL,
Shin LM
(1997)
Functional neuroimaging studies in posttraumatic stress disorder.
In: Psychobiology of posttraumatic stress disorder (Yehuda R,
McFarlane AC,
eds), pp 83-98. New York: New York Academy of Sciences.
-
Rauch SL,
Whalen PJ,
Savage CR,
Curran T,
Kendrick A,
Brown HD,
Bush G,
Breiter HC,
Rosen BR
(1997)
Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging.
Hum Brain Mapp
5:124-132. [Web of Science][Medline]
-
Reese TG,
Davis TL,
Weisskoff RM
(1995)
Automated shimming at 1.5 T using echo-planar image frequency maps.
J Magn Reson Imaging
5:739-745[Web of Science][Medline].
-
Reiman EM,
Lane RD,
Ahern GL,
Schwartz GE,
Davidson RJ,
Friston KJ,
Yun L,
Chen K
(1997)
Neuroanatomical correlates of externally and internally generated human emotion.
Am J Psychiatry
154:918-925[Abstract].
-
Richardson RT,
Mitchell SJ,
Baker FH,
DeLong MR
(1988)
Responses of nucleus basalis of Meynert neurons in behaving monkeys.
In: Cellular mechanisms of conditioning and behavioral plasticity (Woody CD,
Alkon DL,
McGaugh JL,
eds), pp 161-173. New York: Plenum.
-
Roediger HL
(1980)
Memory metaphors in cognitive psychology.
Mem Cognit
8:231-246[Web of Science][Medline].
-
Rolls ET,
Tovee MJ
(1994)
Processing speed in the cerebral cortex and the neurophysiology of visual masking.
Proc R Soc Lond [Biol]
257:9-15[Medline].
-
Russchen FT,
Amaral DG,
Price JL
(1985)
The afferent connections of the substantia innominata in the monkey, Macaca fascicularis.
J Comp Neurol
242:1-27[Web of Science][Medline].
-
Schacter DS,
Chiu P,
Ochsner KN
(1993)
Implicit memory: a selective review.
Annu Rev Neurosci
16:159-182[Web of Science][Medline].
-
Seamon JG,
Williams PC,
Crowley MJ,
Kim IJ,
Langer SA,
Orne PJ,
Wishengrad DL
(1995)
The mere exposure effect is based on implicit memory: effects of stimulus type, encoding conditions and number of exposures on recognition and affect judgments.
J Exp Psychol
21:711-721.
-
Shupp HT,
Cuthbert BN,
Bradley MM,
Birbaumer N,
Lang P
(1997)
Probe P3 and blinks: two measures of affective startle modulation.
Psychophysiology
34:1-6[Web of Science][Medline].
-
Sillitto AM,
Kemp JA
(1983)
Cholinergic modulation of the functional organization of the cat visual cortex.
Brain Res
289:143-155[Web of Science][Medline].
-
Szerb JC
(1967)
Cortical acetylcholine release and electroencephalographic arousal.
J Physiol (Lond)
192:329-345[Abstract/Free Full Text].
-
Talairach J,
Tournoux P
(1988)
In: Co-planar stereotaxic atlas of the human brain. New York: Theime.
-
Tranel D,
Damasio H,
Damasio AR
(1995)
Double dissociation between overt and covert face recognition.
J Cognit Neurosci
7:425-432. [Web of Science]
-
Underwood BJ
(1965)
False recognition produced by implicit verbal responses.
J Exp Psychol
70:122-129.
-
Whalen PJ,
Kapp BS
(1991)
Contributions of the amygdaloid central nucleus to the modulation of the nictitating membrane reflex in the rabbit.
Behav Neurosci
104:141-153.
-
Whalen PJ,
Kapp BS,
Pascoe J
(1994)
Neuronal activity within the nucleus basalis and conditioned neocortical electroencephalographic activation.
J Neurosci
14:1623-1633[Abstract].
-
Wilson FAW,
Rolls ET
(1990)
Neuronal responses related to reinforcement in the primate basal forebrain.
Exp Brain Res
509:213-231.
-
Woods RP,
Cherry SR,
Mazziotta JC
(1992)
Automated algorithm for aligning tomographic images. II. Cross-modality MRI-PET registration.
J Comput Assist Tomogr
16:620-633[Web of Science][Medline].
-
Zajonc RB
(1980)
Feeling and thinking: preferences need no inferences.
Am Psychologist
35:151-175.
Copyright © 1998 Society for Neuroscience 0270-6474/98/181411-08$05.00/0
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|
|
|
|
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|
|
|
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|
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|
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|
|
|
|
|
|
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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Capturing and holding attention: The impact of emotional words in rapid serial visual presentation
Mem Cognit,
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36(1):
182 - 200.
[Abstract]
[PDF]
|
|
|
|
|
|
|
C. S. Monk, R. G. Klein, E. H. Telzer, E. A. Schroth, S. Mannuzza, J. L. Moulton III, M. Guardino, C. L. Masten, E. B. McClure-Tone, S. Fromm, et al.
Amygdala and Nucleus Accumbens Activation to Emotional Facial Expressions in Children and Adolescents at Risk for Major Depression
Am J Psychiatry,
January 1, 2008;
165(1):
90 - 98.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. L. Keightley, K. S. Chiew, G. Winocur, and C. L. Grady
Age-related differences in brain activity underlying identification of emotional expressions in faces
Soc Cogn Affect Neurosci,
December 1, 2007;
2(4):
292 - 302.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. V. Rauch, P. Ohrmann, J. Bauer, H. Kugel, A. Engelien, V. Arolt, W. Heindel, and T. Suslow
Cognitive Coping Style Modulates Neural Responses to Emotional Faces in Healthy Humans: A 3-T fMRI Study
Cereb Cortex,
November 1, 2007;
17(11):
2526 - 2535.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Akiyama, M. Kato, T. Muramatsu, S. Umeda, F. Saito, and H. Kashima
Unilateral Amygdala Lesions Hamper Attentional Orienting Triggered by Gaze Direction
Cereb Cortex,
November 1, 2007;
17(11):
2593 - 2600.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Herde, C. Forster, M. Strupf, and H. O. Handwerker
Itch Induced by a Novel Method Leads to Limbic Deactivations A Functional MRI Study
J Neurophysiol,
October 1, 2007;
98(4):
2347 - 2356.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. LeDoux
Unconscious and conscious contributions to the emotional and cognitive aspects of emotions: a comment on Scherer's view of what an emotion is
Social Science Information,
September 1, 2007;
46(3):
395 - 405.
[PDF]
|
|
|
|
|
|
|
W. D. S. Killgore and D. A. Yurgelun-Todd
The right-hemisphere and valence hypotheses: could they both be right (and sometimes left)?
Soc Cogn Affect Neurosci,
September 1, 2007;
2(3):
240 - 250.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Williams and E. Gordon
Dynamic Organization of the Emotional Brain: Responsivity, Stability, and Instability
Neuroscientist,
August 1, 2007;
13(4):
349 - 370.
[Abstract]
[PDF]
|
|
|
|
|
|
|
D. G. Amen, C. Hanks, J. R. Prunella, and A. Green
An Analysis of Regional Cerebral Blood Flow in Impulsive Murderers Using Single Photon Emission Computed Tomography
J Neuropsychiatry Clin Neurosci,
August 1, 2007;
19(3):
304 - 309.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. J. Bishop, R. Jenkins, and A. D. Lawrence
Neural Processing of Fearful Faces: Effects of Anxiety are Gated by Perceptual Capacity Limitations
Cereb Cortex,
July 1, 2007;
17(7):
1595 - 1603.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. F. Barrett, E. Bliss-Moreau, S. L. Duncan, S. L. Rauch, and C. I. Wright
The amygdala and the experience of affect
Soc Cogn Affect Neurosci,
June 1, 2007;
2(2):
73 - 83.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. van der Gaag, R. B. Minderaa, and C. Keysers
The BOLD signal in the amygdala does not differentiate between dynamic facial expressions
Soc Cogn Affect Neurosci,
June 1, 2007;
2(2):
93 - 103.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Lanteaume, S. Khalfa, J. Regis, P. Marquis, P. Chauvel, and F. Bartolomei
Emotion Induction After Direct Intracerebral Stimulations of Human Amygdala
Cereb Cortex,
June 1, 2007;
17(6):
1307 - 1313.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Kouider and S. Dehaene
Levels of processing during non-conscious perception: a critical review of visual masking
Phil Trans R Soc B,
May 29, 2007;
362(1481):
857 - 875.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. F. Baumeister, K. D. Vohs, C. Nathan DeWall, and Liqing Zhang
How Emotion Shapes Behavior: Feedback, Anticipation, and Reflection, Rather Than Direct Causation
Personality and Social Psychology Review,
May 1, 2007;
11(2):
167 - 203.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Bray and J. O'Doherty
Neural Coding of Reward-Prediction Error Signals During Classical Conditioning With Attractive Faces
J Neurophysiol,
April 1, 2007;
97(4):
3036 - 3045.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Olsson, K. I. Nearing, and E. A. Phelps
Learning fears by observing others: the neural systems of social fear transmission
Soc Cogn Affect Neurosci,
March 15, 2007;
(2007)
nsm005v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. B. Stein, A. N. Simmons, J. S. Feinstein, and M. P. Paulus
Increased Amygdala and Insula Activation During Emotion Processing in Anxiety-Prone Subjects
Am J Psychiatry,
February 1, 2007;
164(2):
318 - 327.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. M. Gothard, F. P. Battaglia, C. A. Erickson, K. M. Spitler, and D. G. Amaral
Neural Responses to Facial Expression and Face Identity in the Monkey Amygdala
J Neurophysiol,
February 1, 2007;
97(2):
1671 - 1683.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Skuse
Genetic influences on the neural basis of social cognition
Phil Trans R Soc B,
December 29, 2006;
361(1476):
2129 - 2141.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. H. Somerville and P. J. Whalen
Prior experience as a stimulus category confound: an example using facial expressions of emotion
Soc Cogn Affect Neurosci,
December 1, 2006;
1(3):
271 - 274.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. K. Anderson, Y. Yamaguchi, W. Grabski, and D. Lacka
Emotional memories are not all created equal: Evidence for selective memory enhancement
Learn. Mem.,
November 1, 2006;
13(6):
711 - 718.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Williams, P. Das, B. J. Liddell, A. H. Kemp, C. J. Rennie, and E. Gordon
Mode of Functional Connectivity in Amygdala Pathways Dissociates Level of Awareness for Signals of Fear
J. Neurosci.,
September 6, 2006;
26(36):
9264 - 9271.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Gaillard, A. Del Cul, L. Naccache, F. Vinckier, L. Cohen, and S. Dehaene
Nonconscious semantic processing of emotional words modulates conscious access
PNAS,
May 9, 2006;
103(19):
7524 - 7529.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Pessoa, S. Japee, D. Sturman, and L. G. Ungerleider
Target Visibility and Visual Awareness Modulate Amygdala Responses to Fearful Faces
Cereb Cortex,
March 1, 2006;
16(3):
366 - 375.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Suzuki, T. Hoshino, K. Shigemasu, and M. Kawamura
Disgust-specific impairment of facial expression recognition in Parkinson's disease
Brain,
March 1, 2006;
129(3):
707 - 717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. F. Barrett
Solving the Emotion Paradox: Categorization and the Experience of Emotion
Personality and Social Psychology Review,
February 1, 2006;
10(1):
20 - 46.
[Abstract]
[PDF]
|
|
|
|
|
|
|
A. K. Anderson, P. E. Wais, and J. D. E. Gabrieli
Emotion enhances remembrance of neutral events past
PNAS,
January 31, 2006;
103(5):
1599 - 1604.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Schacher, B. Haemmerle, F. G. Woermann, M. Okujava, D. Huber, T. Grunwald, G. Kramer, and H. Jokeit
Amygdala fMRI lateralizes temporal lobe epilepsy
Neurology,
January 10, 2006;
66(1):
81 - 87.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. de Gelder, J. S. Morris, and R. J. Dolan
Unconscious fear influences emotional awareness of faces and voices
PNAS,
December 20, 2005;
102(51):
18682 - 18687.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Kirsch, C. Esslinger, Q. Chen, D. Mier, S. Lis, S. Siddhanti, H. Gruppe, V. S. Mattay, B. Gallhofer, and A. Meyer-Lindenberg
Oxytocin Modulates Neural Circuitry for Social Cognition and Fear in Humans
J. Neurosci.,
December 7, 2005;
25(49):
11489 - 11493.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. F Green, B. Olivier, J. N Crawley, D. L Penn, and S. Silverstein
Social Cognition in Schizophrenia: Recommendations from the Measurement and Treatment Research to Improve Cognition in Schizophrenia New Approaches Conference
Schizophr Bull,
October 1, 2005;
31(4):
882 - 887.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. S. Winston, J. A. Gottfried, J. M. Kilner, and R. J. Dolan
Integrated Neural Representations of Odor Intensity and Affective Valence in Human Amygdala
J. Neurosci.,
September 28, 2005;
25(39):
8903 - 8907.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Jolij and V. A. F. Lamme
Repression of unconscious information by conscious processing: Evidence from affective blindsight induced by transcranial magnetic stimulation
PNAS,
July 26, 2005;
102(30):
10747 - 10751.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Naccache, R. Gaillard, C. Adam, D. Hasboun, S. Clemenceau, M. Baulac, S. Dehaene, and L. Cohen
A direct intracranial record of emotions evoked by subliminal words
PNAS,
May 24, 2005;
102(21):
7713 - 7717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. D. De Bellis
The Psychobiology of Neglect
Child Maltreat,
May 1, 2005;
10(2):
150 - 172.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. S. Milak, R. V. Parsey, J. Keilp, M. A. Oquendo, K. M. Malone, and J. J. Mann
Neuroanatomic Correlates of Psychopathologic Components of Major Depressive Disorder
Arch Gen Psychiatry,
April 1, 2005;
62(4):
397 - 408.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. M. Shin, C. I. Wright, P. A. Cannistraro, M. M. Wedig, K. McMullin, B. Martis, M. L. Macklin, N. B. Lasko, S. R. Cavanagh, T. S. Krangel, et al.
A Functional Magnetic Resonance Imaging Study of Amygdala and Medial Prefrontal Cortex Responses to Overtly Presented Fearful Faces in Posttraumatic Stress Disorder
Arch Gen Psychiatry,
March 1, 2005;
62(3):
273 - 281.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Gosselin, I. Peretz, M. Noulhiane, D. Hasboun, C. Beckett, M. Baulac, and S. Samson
Impaired recognition of scary music following unilateral temporal lobe excision
Brain,
March 1, 2005;
128(3):
628 - 640.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. A. Miller, K. H. Taber, G. O. Gabbard, and R. A. Hurley
Neural Underpinnings of Fear and Its Modulation: Implications for Anxiety Disorders
J Neuropsychiatry Clin Neurosci,
February 1, 2005;
17(1):
1 - 6.
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Winkielman, K. C. Berridge, and J. L. Wilbarger
Unconscious Affective Reactions to Masked Happy Versus Angry Faces Influence Consumption Behavior and Judgments of Value
Pers Soc Psychol Bull,
January 1, 2005;
31(1):
121 - 135.
[Abstract]
[PDF]
|
|
|
|
|
|
|
P. J. Whalen, J. Kagan, R. G. Cook, F. C. Davis, H. Kim, S. Polis, D. G. McLaren, L. H. Somerville, A. A. McLean, J. S. Maxwell, et al.
Human Amygdala Responsivity to Masked Fearful Eye Whites
Science,
December 17, 2004;
306(5704):
2061 - 2061.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Pierce, F. Haist, F. Sedaghat, and E. Courchesne
The brain response to personally familiar faces in autism: findings of fusiform activity and beyond
Brain,
December 1, 2004;
127(12):
2703 - 2716.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. J. Bishop, J. Duncan, and A. D. Lawrence
State Anxiety Modulation of the Amygdala Response to Unattended Threat-Related Stimuli
J. Neurosci.,
November 17, 2004;
24(46):
10364 - 10368.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. M. Pause, A. Ohrt, A. Prehn, and R. Ferstl
Positive Emotional Priming of Facial Affect Perception in Females is Diminished by Chemosensory Anxiety Signals
Chem Senses,
November 1, 2004;
29(9):
797 - 805.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-P. Royet and J. Plailly
Lateralization of Olfactory Processes
Chem Senses,
October 1, 2004;
29(8):
731 - 745.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. R. Herbert
Neuroimaging in Disorders of Social and Emotional Functioning: What Is the Question?
J Child Neurol,
October 1, 2004;
19(10):
772 - 784.
[Abstract]
[PDF]
|
|
|
|
|
|
|
J. S. Winston, R.N.A. Henson, M. R. Fine-Goulden, and R. J. Dolan
fMRI-Adaptation Reveals Dissociable Neural Representations of Identity and Expression in Face Perception
J Neurophysiol,
September 1, 2004;
92(3):
1830 - 1839.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Pare, G. J. Quirk, and J. E. Ledoux
New Vistas on Amygdala Networks in Conditioned Fear
J Neurophysiol,
July 1, 2004;
92(1):
1 - 9.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Nofzinger, D. J. Buysse, A. Germain, C. Carter, B. Luna, J. C. Price, C. C. Meltzer, J. M. Miewald, C. F. Reynolds III, and D. J. Kupfer
Increased Activation of Anterior Paralimbic and Executive Cortex From Waking to Rapid Eye Movement Sleep in Depression
Arch Gen Psychiatry,
July 1, 2004;
61(7):
695 - 702.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Ishai, L. Pessoa, P. C. Bikle, and L. G. Ungerleider
Repetition suppression of faces is modulated by emotion
PNAS,
June 29, 2004;
101(26):
9827 - 9832.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. S. Heberlein and R. Adolphs
Impaired spontaneous anthropomorphizing despite intact perception and social knowledge
PNAS,
May 11, 2004;
101(19):
7487 - 7491.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Izquierdo and E. A. Murray
Combined Unilateral Lesions of the Amygdala and Orbital Prefrontal Cortex Impair Affective Processing in Rhesus Monkeys
J Neurophysiol,
May 1, 2004;
91(5):
2023 - 2039.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Williams, A. P. Morris, F. McGlone, D. F. Abbott, and J. B. Mattingley
Amygdala Responses to Fearful and Happy Facial Expressions under Conditions of Binocular Suppression
J. Neurosci.,
March 24, 2004;
24(12):
2898 - 2904.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Kensinger and S. Corkin
Two routes to emotional memory: Distinct neural processes for valence and arousal
PNAS,
March 2, 2004;
101(9):
3310 - 3315.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K Dujardin, S Blairy, L Defebvre, P Krystkowiak, U Hess, S Blond, and A Destee
Subthalamic nucleus stimulation induces deficits in decoding emotional facial expressions in Parkinson's disease
J. Neurol. Neurosurg. Psychiatry,
February 1, 2004;
75(2):
202 - 208.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Glascher and R. Adolphs
Processing of the Arousal of Subliminal and Supraliminal Emotional Stimuli by the Human Amygdala
J. Neurosci.,
November 12, 2003;
23(32):
10274 - 10282.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
Top
Abstract
Introduction
