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Research Paper
Sex-Related Hemispheric Lateralization of Amygdala Function in Emotionally Influenced Memory: An fMRI Investigation
1 Center for the Neurobiology of Learning and Memory and Department of Neurobiology and Behavior,2 Department of Anesthesiology, and3 Department of Psychiatry and Human Behavior, University of California, Irvine, California, 92697-3800, USA
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ABSTRACT |
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 TOP ABSTRACT RESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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) and human
(Cahill 2000) subject studies.
For example, activity of the human amygdala during encoding of arousing
material relates significantly to long-term memory of that material but not to
memory of nonarousing material (Cahill et al.
1996,
2001; Canli et al.
1999,
2000,
2002;
Hamann et al. 1999).
Conversely, bilateral amygdala lesions reduce or abolish enhanced long-term
memory associated with emotional arousal, although they do not affect memory
for relatively neutral material or affect emotional reactions per se to
arousing stimuli (Cahill et al. 2000).
More recently, human brain imaging evidence has begun to reveal a
sex-related hemispheric lateralization of amygdala function with respect to
memory for emotionally arousing material. For example, in both a glucose PET
investigation (Cahill et al.
2001) and an fMRI investigation
(Canli et al. 2002), activity
of the right, but not left, hemisphere amygdala related significantly to
long-term incidental memory for arousing material in men but not in women,
whereas activity of the left, but not right, hemisphere amygdala related
significantly to memory for arousing material in women but not in men. As
noted recently by Pizzagalli and colleagues
(2003), such claims about
lateralized amygdala function "require systematic replication."
Providing such a replication was the first major aim of the present study.
Evidence for hemispheric lateralization of brain function derived from
brain imaging investigations must be approached with caution, as thresholding
differences may create the appearance of asymmetrical function greater than
that which actually exists. One method to further substantiate the existence
of a sex-related hemispheric lateralization of amygdala function with respect
to memory for arousing material is to demonstrate the existence of a
sex-by-hemisphere interaction in this relationship
(Pizzagalli et al. 2003),
which no previous study of the amygdala sex-related lateralization in relation
to memory has reported. This issue is perhaps of even greater importance in
considering regions, such as the amygdala, that are prone to susceptibility
artifacts and reduced signal-to-noise ratio with functional Magnetic Resonance
Imaging (fMRI) (LaBar et al.
2001). Thus, a second major aim of the present study was to
document the existence of a sex-by-hemisphere interaction in amygdala function
in emotionally influenced memory. The study procedures were patterned after an
earlier fMRI investigation of amygdala function in emotionally influenced
memory (Canli et al.
2000).
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RESULTS |
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TOPABSTRACTRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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Sex-related differences in the arousal ratings of the pictures were
consistent with those found by Canli et al.
(2002). Specifically, women
rated more pictures as most highly arousing (rating of four) than did men
(t(21) = -1.82, P = 0.04). And similar to the findings of Canli et
al. (2002), there were no
sex-related differences in the number of false recollections (F(1,21) = 0.47,
P > 0.05; 19% for men and 16% for women). Also, significant
sex-related differences in memory performance existed only for pictures rated
as most highly arousing. However, unlike the study of Canli et al.
(2002), in the present study
men exhibited better retention than did women for the most arousing pictures.
Specifically, men recalled a higher percentage of pictures rated as most
highly arousing (t(21) = 2.04, P = 0.05;
Fig. 1A) than did women. Men
also remembered with certainty a higher percentage of pictures rated most
highly arousing (t(21) = 2.07, P = 0.05;
Fig. 1B.) Both sexes remembered
a higher percentage of pictures rated as highly arousing than a percentage of
pictures rated as not arousing at all (t(20) = -3.05, P = 0.01 for
women; t(22) = -3.81, P = 0.001 for men).
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Amygdala Function
The results of the between-groups, random-effects analysis comparing women and men are shown in Figure 2. In women, the left hemisphere amygdala, but not the right, demonstrated greater blood oxygen level-dependent (BOLD) signal with better memory performance and increasing arousal ratings than occurred in men. In contrast, in men the right hemisphere amygdala, but not the left, demonstrated greater BOLD signal with better memory performance and increasing arousal ratings than occurred in women. In addition, the significant amygdala activation was more medial in women than it was in men, with the peak activation located 4 mm more medially in women than in men.
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Analysis of amygdala activity independently in men and women revealed
significant activation clusters in the right but not left hemisphere amygdala
in men, and in the left but not right hemisphere amygdala in women (P
< 0.001, uncorrected for multiple comparisons). These results are shown in
Figure 3A. The results of the
sex-by-hemisphere ANOVA on the parameter estimates of amygdala activity
revealed a significant interaction between sex and hemisphere (F(1,13) = 7.99,
P = 0.022; Fig. 3B). The additional ANOVA using parameter estimates from amygdala voxel coordinates
derived from an independent study of amygdala participation in emotionally
influenced memory (Canli et al.
2002) also revealed a significant sex-by-hemisphere interaction
(F(1,13) = 6.35, P = 0.026).
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Although not central to the primary amygdala question at issue in this study, the within-groups analysis also revealed other brain regions demonstrating significantly greater BOLD signal with both better subsequent memory and increasing arousal ratings. All such significant regions with a minimum voxel cluster size of four voxels are listed in Table 1. Men showed significant (P < 0.001) activations including the right anterior hippocampus, right globus pallidus, bilateral lateral parietal, and right frontal cortex. Four out of six significant activations in men were located in the right hemisphere. In contrast, all significant activations detected in women were located in the left hemisphere, including the left posterior cingulate, left middle temporal gyrus, and left inferior parietal cortex.
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DISCUSSION |
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TOPABSTRACTRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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). For the
left hemisphere amygdala, a significantly stronger relationship between its
activity at encoding and long-term memory for arousing pictures was detected
in women relative to men, although no such difference occurred in the right
hemisphere amygdala. Conversely, for the right hemisphere amygdala, a
significantly stronger relationship between its activity at encoding and
long-term memory for arousing pictures was detected in men relative to women,
although no such difference occurred in the left hemisphere amygdala. A second
analysis independently assessing the group activity of the amygdala in men and
women confirmed this result, including documentation of a significant
sex-by-hemisphere interaction in the amygdala relationship to memory for
arousing pictures. These results provide the most compelling demonstration to
date of a sex-related hemispheric lateralization of amygdala function in
memory for emotionally arousing events and, together with previous studies
(Cahill et al. 1996,
2001; Canli et al.
1999,
2000,
2002;
Hamann et al. 1999), leave no
reasonable doubt about the existence of this sex-related laterality in humans,
at least as regards negatively valenced material.
Several points concerning this lateralization should be emphasized. First,
the consistent amygdala lateralization seen to date has been in its
relationship to long-term memory for emotionally arousing events, as
opposed to its relation to emotional reactions per se. Canli et al.
(2002), for example, found
that activity of the left amygdala related to emotional reactions to pictures
in both men and women, despite that fact that they also found a very similar
sex-related hemispheric lateralization of amygdala function with respect to
memory as reported here. Second, we emphasize that our findings do not
indicate that the left hemisphere amygdala in men and the right hemisphere
amygdala in women have no function(s) in memory. They indicate only that there
is a significant lateralization of these functions, at least with respect to
the type of information learned in this experiment. Third, and related to the
second point, we emphasize that all experiments to date in which the
sex-related lateralization was found, including this experiment, involved
emotionally negative material. Although we argue that arousal, rather than
valence, is the key to amygdala engagement in memory processes
(Cahill and McGaugh 1990;
Cahill 2000), it may be that an
identical sex-related lateralization of amygdala function will not exist in
similarly arousing but emotionally positive learning situations.
Although the evidence to date points compellingly to the existence of a
sex-related hemispheric lateralization of amygdala function in relation to
memory for emotional events, it does not yet clarify what this lateralization
means and what combination of biological (nature) and psychological (nurture)
factors produced it. Answering these questions is now crucial for future
investigation. One hypothesis we have pursued in this regard concerns
hemispheric specialization in the processing of relatively global holistic
aspects of a stimulus or scene versus processing of relative local
fine-detailed aspects of the stimulus or scene. Substantial evidence points to
a bias of the right hemisphere in processing global information and to a bias
of the left hemisphere in processing local information (see
Delis et al. 1986;
Fink et al. 1997;
Ivry and Robertson 1998). We
combined this fact with the sex-related hemispheric specialization of the
amygdala ("males right/females left") to detect a sex-related
difference in the impairing effect of a drug that presumably impairs amygdala
function in memory, the ß-adrenergic antagonist propranolol
(Cahill and van Stegeren 2003).
It appears that couching our understanding of amygdala function in terms of
the hemisphere in which each amygdala operates is one method to begin to
understand the functional significance of the sex-related amygdala
lateralization in memory.
The "memory modulation" hypothesis of amygdala function
(McGaugh 2000) requires that
the amygdala work in concert with other brain regions to influence memory.
Although the focus of this article is the amygdala, our analyses revealed
other brain regions with activity that is similarly related to memory
(Table 1). Interestingly, six
out of eight significant activations in men were located in the right
hemisphere. In contrast, all significant activations detected in women were
located in the left hemisphere. It is also of interest that right hemisphere
hippocampal and frontal regions in men showed activation patterns similar to
those of the right amygdala. A recent study from our laboratory
(Kilpatrick and Cahill 2003)
provided the first evidence of heightened outflow from the amygdala to other
brain regions in emotional compared with neutral learning conditions, most
notably from the right hemisphere amygdala in men to ipsilateral frontal and
parahippocampal regions.
A steadily growing number of studies indicate sex-related influences on
amygdala function. For example, Killgore and colleagues
(2001) report sex-related
differences in amygdala responsiveness to faces, whereas an extensive series
of studies by the Gurs and their colleagues
(Gur et al. 2002) documents
sex-related differences in many aspects of brain function, including the size
of the amygdala relative to other brain regions. Similarly Giedd and
colleagues (1997) found a
sex-related difference in the relative sizes of the amygdala and hippocampus.
The amygdala is larger relative to total cerebral size in men compared with
women, and in boys compared with girls
(Durston et al. 2001;
Goldstein et al. 2001).
Zubieta and colleagues (1999)
found significant sex-related differences in opioid receptor binding within
the amygdale. A recent meta-analysis of the literature by Wager et al.
(2003) identified a
female-left/male-right lateralization of an "extended amygdala"
area in relation to emotional arousal. And recently, Toufexis and Davis
(2002) reported a pronounced
influence both of sex and of the sex hormone progesterone on an
amygdala-dependent process-fear potentiated startle in rats. Finally,
intravenous administration of procaine, which can produce a dramatic emotional
response, produced significantly greater left amygdala activation in women
compared with men (Adinoff et al.
2003). The issue of sex-related influences may also inform other
views of amygdala functional hemispheric specialization
(Morris et al. 1998;
Buchanan et al. 2001;
Phelps et al. 2001), none of
which to date have accounted for potential influences of sex.
It is possible that the sex-related differences in recognition memory
performance seen in the present study and the one by Canli et al.
(2000,
2002) are at least partially
related to sex-related differences in response bias. For example, the current
data cannot eliminate the possibility that the male's higher hit rate for
highly arousing pictures was due in part to an increased bias to respond
"old" to any emotionally arousing picture (foils as well as
targets). Measures such as d' are designed to account for such
differences in response biases by considering a subject's false alarm rate as
well as their hit rate. d' could not be computed in the current study as
the lack of arousal ratings for the foils rendered it impossible to determine
the subject's false alarm rate for each arousal level. Future studies should
include subject ratings for the foils used on recognition tests. Although the
present study cannot rule out the influence of response bias, the sex-related
lateralization of amygdala function reported here is entirely consistent with
that of our earlier investigation using free recall tests
(Cahill et al. 2001), in which
response bias could not account for the findings.
In conclusion, the present findings provide the most compelling
demonstration to date of a sex-related hemispheric lateralization of amygdala
function with respect to memory for emotionally arousing events. As such, they
strengthen the argument that a complete understanding of neurobiological
mechanisms underlying emotionally influenced memory now requires that we
anticipate, and account for, the influence of sex
(Shors 1998;
Cahill et al. 2001) or gender
(Cahill et al. 2004).
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MATERIALS AND METHODS |
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TOPABSTRACTRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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Twenty-three right-handed healthy volunteers (12 male; 11 female) participated in this study. The average age of the male subjects was 26.0 ± 5.4 years, and the average age of the female subjects was 23.6 ± 3.5 years. Subjects had no history of head injury, mental illness, or substance abuse, or had any counter indications for MRI. Subjects were recruited through posted advertisements and paid 40 dollars for their participation. All subjects were treated in accordance with the approved procedures of the institutional review boards of both the Veterans Affairs Medical Center in Long Beach, California, and the University of California-Irvine. A total of eight subjects were removed for the imaging analysis: four men and four women. Two of the women were removed for signal dropout in the medial temporal lobes, and the rest (four men, two women) were removed for movement >3 mm, leaving a total of 15 subjects (eight men and seven women) in the imaging analysis.
Behavioral Procedures
The stimuli were those described by Canli et al.
(2000), with some
modifications in the manner in which they were presented. Subjects viewed 96
scenes from the International Affective Picture System (IAPS) stimuli set. The
normative valence ratings for this set ranged from highly negative (1.17) to
neutral (5.44), and the normative arousal ratings ranged from tranquil (1.97)
to highly arousing (7.63). Further details regarding this set can be found in
Canli et al. (2000). In the
present experiment, the 96 scenes were presented in three blocks of 32 scenes
matched in terms of normative arousal ratings. The order of the blocks was
counterbalanced across subjects, and within each block, the order of scenes
was randomized across subjects. Each scene was presented for 2.88 sec with an
interstimulus interval of 12.96 sec, during which subjects viewed a fixation
cross. Subjects were asked to indicate their emotional arousal after the scene
disappeared by pressing a lever with their right hand. Subjects chose from
four levers, indicating emotional arousal on a scale of one ("not
emotionally arousing") to four ("highly emotionally
arousing"). The subject's responses were recorded by the
experimenter.
Two weeks after the scan, subjects received an unexpected recognition test
in a room next to the scanner. During the recognition test, subjects viewed
all of the previously seen pictures and 48 new IAPS scenes (foils) on a Dell
Inspiron 8100. The foils were selected to match the previously seen pictures
in their normative valence and arousal ratings (for details regarding this
set, see Canli et al. 2000).
Subjects were asked whether they had seen the picture during the scan 2 weeks
earlier. When the subject judged a picture as previously seen, they were then
asked to indicate whether they remembered with certainty
("remember") or had a less certain feeling of familiarity
("know"). Subjects also completed the Mehrabian scale designed to
assess trait arousability (Mehrabian
1977), although these data were not included in the analyses.
Scanning Procedures
Data were acquired at the Long Beach Veterans Affairs Medical Center in a 1.5T scanner manufactured by Marconi Medical Systems, Inc., with multislice echo-planar imaging capabilities developed and installed by Marconi. This system was used to acquire both T1-weighted anatomical volume images and T2*-weighted functional images with BOLD contrast. For each session, the magnetic gradient was automatically shimmed by using a first-order algorithm with the subject's head centered in the magnetic field. A high-resolution full-brain anatomical image was acquired for each subject at the beginning of each session.
Anatomical images were acquired by using a Fourier-acquired steady-state technique (FAST) sequence with an in-plane resolution of 0.94 x 0.94 mm2 and a slice thickness of 2.5 mm. Functional images were acquired by using a gradient-echo echo-planar imaging sequence (TR = 1.807 sec, TE = 40 msec, flip angle = 90 degrees, fat-saturating prepulse). Each echo planar image consisted of sixteen 7-mm axial slices of in-plane voxel size 1.88 x 1.88 mm2. Three runs of 289 volumes each were collected continuously. The first three volumes in each run were discarded to account for T1 equilibration effects.
Stimuli were presented via MRI-compatible Silent Vision goggles. Silent Scan headphones from Avotec were used to communicate with participants in the scanner. While they were in the scanner, subjects wore earplugs and headphones. Head motion was reduced by lining the head coil with pads, taping subjects heads to the head coil, and instructing subjects to lie as still as possible in particular during actual scanning sequences.
Data Analysis
Image processing and statistical analyses were carried out by using the
Statistical Parametric Mapping (SPM99) analysis package
(http://www.fil.ion.ucl.ac.uk/spm)
and MATLAB software (The MathWorks). Following standard functional image
processing and analysis procedures, all volumes from each subject were
realigned by using the first volume as a reference, and resliced by using sinc
interpolation. The functional images were coregistered to the corresponding
anatomical (T1-weighted) image, spatially normalized into standard
stereotactic space (Friston et al.
1995) with respect to the MNI-305 template (Montreal Neurological
Institute) applying nonlinear basis functions, and spatially smoothed by using
an 8-mm FWHM isotropic Gaussian kernel. The time-series images were then
high-pass filtered by using a discrete set of nonlinear basis functions with a
cutoff period of 1/120 Hz to eliminate low-frequency periodicities, and scaled
within-session to a grand mean of 100. For temporal smoothing, the covariates
were convolved with a canonical hemodynamic response function. Those subjects
whose movement exceeded 3 mm (n = 5) were omitted from the analysis. In
addition, to ensure that sufficient signal was obtained from all relevant
amygdala voxels, a standard global mask (grey matter threshold) was applied to
all voxels. This was done in SPM99 by (1) calculating the mean intensity of
all voxels, (2) discarding any voxels with less than one-eighth of this mean,
(3) calculating a new voxel mean (termed the global mean), and (4) including
in the analysis only those voxels with signal >0.8 of the global mean.
A voxelwise application of the general linear model to the time series
images determined parameter estimates and variance for each covariate in a
subject-specific fixed effects model. Intersubject variance was modeled in a
random effects (second level) model
(Friston et al. 1999). The
variance in BOLD signal for each subject was decomposed into a set of
regressors associated with arousal-related activity and subsequent memory
performance-related activity. We identified regions showing emotional
arousal-related modulation of memory-related activity by decomposing the
variance in BOLD signal for each subject into event-related regressors and
corresponding parametric modulatory regressors. To do so, stimuli were
classified into three event-types of interest: high confidence hits, low
confidence hits, and misses. The magnitude of the BOLD response to each event
was modeled by convolving a 
function at each event onset with a
canonical hemodynamic response function. An additional regressor for each
event-type of corresponding emotional arousal ratings was used to model the
parametric modulation of subsequent recognition performance by emotional
arousal rating using a linear function. The contrast of the difference in
modulatory regressors across memory performance levels identified regions
where greater BOLD signal was associated with both better memory performance
and increasing arousal ratings. Given our hypothesis regarding the effect of
arousal and subsequent memory within the amygdala, a region of interest
analysis was performed with small volume correction for multiple comparisons
(sphere radius = 5 mm), centering on those voxels in the amygdala that showed
significant activations in the specified model
(Worsley et al. 1996).
To provide additional documentation of a sex-related hemispheric
lateralization of amygdala function in relation to memory for arousing
stimuli, a sex-by-hemisphere ANOVA was performed. To obtain parameter
estimates for the height of the BOLD response for men and women, each group
was analyzed independently with the contrast described above (the parametric
modulation of memory by arousal) in a random-effects analysis. The parameter
estimates of the independent group analyses were adjusted for confounds and
fitted to the group grand mean. The adjusted parameter estimates from each
group's maximally activated voxel within each subject's amygdala were used to
analyze interactions between sex and hemisphere. A liberal statistical
threshold (P < 0.3) was needed to obtain parameter estimates from
the homotopic voxel in the amygdala of opposing hemisphere (left in men, right
in women). Thus, two values were obtained for each subject: the ß at the
peak voxel and the ß for the homotopic voxel in the opposite hemisphere.
These betas constituted the dependent variables in a 2 x 2
repeated-measures ANOVA. To avoid bias because parameter estimates were
selected based on activations from the above contrast, a second ANOVA was
performed using amygdala voxel coordinates from a previous study
(Canli et al, 2002).
Behavioral data concerning arousal ratings and memory were investigated by
using ANOVA and unpaired t-tests.
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ACKNOWLEDGMENTS |
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The publication costs of this article were defrayed in part by payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 USC section 1734 solely to indicate this fact.
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FOOTNOTES |
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4 E-MAIL lfcahill{at}uci.edu; FAX (949) 824-5244.
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  T. Sommer, J. Glascher, S. Moritz, and C. Buchel Emotional enhancement effect of memory: Removing the influence of cognitive factors Learn. Mem., August 6, 2008; 15(8): 569 - 573. [Abstract] [Full Text] [PDF]
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 K. McRae, K. N. Ochsner, I. B. Mauss, J. J. D. Gabrieli, and J. J. Gross Gender Differences in Emotion Regulation: An fMRI Study of Cognitive Reappraisal Group Processes Intergroup Relations, April 1, 2008; 11(2): 143 - 162. [Abstract] [PDF]
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D. Talmi, A. K. Anderson, L. Riggs, J. B. Caplan, and M. Moscovitch Immediate memory consequences of the effect of emotion on attention to pictures Learn. Mem., March 5, 2008; 15(3): 172 - 182. [Abstract] [Full Text] [PDF]
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 M. T. Alkire, R. Gruver, J. Miller, J. R. McReynolds, E. L. Hahn, and L. Cahill Neuroimaging analysis of an anesthetic gas that blocks human emotional memory PNAS, February 5, 2008; 105(5): 1722 - 1727. [Abstract] [Full Text] [PDF]
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 M. Reuber, S. Howlett, A. Khan, and R. A. Grunewald Non-Epileptic Seizures and Other Functional Neurological Symptoms: Predisposing, Precipitating, and Perpetuating Factors Psychosomatics, June 1, 2007; 48(3): 230 - 238. [Abstract] [Full Text] [PDF]
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 Y. Carrasquillo and R. W. Gereau IV Activation of the Extracellular Signal-Regulated Kinase in the Amygdala Modulates Pain Perception J. Neurosci., February 14, 2007; 27(7): 1543 - 1551. [Abstract] [Full Text] [PDF]
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K. L. Mackiewicz, I. Sarinopoulos, K. L. Cleven, and J. B. Nitschke The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory PNAS, September 19, 2006; 103(38): 14200 - 14205. [Abstract] [Full Text] [PDF]
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S. Steidl, S. Mohi-uddin, and A. K. Anderson Effects of emotional arousal on multiple memory systems: Evidence from declarative and procedural learning Learn. Mem., September 1, 2006; 13(5): 650 - 658. [Abstract] [Full Text] [PDF]
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 K. Sergerie, M. Lepage, and J. L. Armony A Process-specific Functional Dissociation of the Amygdala in Emotional Memory. J. Cogn. Neurosci., August 1, 2006; 18(8): 1359 - 1367. [Abstract] [Full Text] [PDF]
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Y. R. Smith, C. S. Stohler, T. E. Nichols, J. A. Bueller, R. A. Koeppe, and J.-K. Zubieta Pronociceptive and Antinociceptive Effects of Estradiol through Endogenous Opioid Neurotransmission in Women J. Neurosci., May 24, 2006; 26(21): 5777 - 5785. [Abstract] [Full Text] [PDF]
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 T. W. Buchanan, D. Tranel, and R. Adolphs Memories for emotional autobiographical events following unilateral damage to medial temporal lobe Brain, January 1, 2006; 129(1): 115 - 127. [Abstract] [Full Text] [PDF]
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D. Tranel, H. Damasio, N. L. Denburg, and A. Bechara Does gender play a role in functional asymmetry of ventromedial prefrontal cortex? Brain, December 1, 2005; 128(12): 2872 - 2881. [Abstract] [Full Text] [PDF]
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A. Mechelli, K. J. Friston, R. S. Frackowiak, and C. J. Price Structural Covariance in the Human Cortex J. Neurosci., September 7, 2005; 25(36): 8303 - 8310. [Abstract] [Full Text] [PDF]
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R. T. LaLumiere and J. L. McGaugh Memory enhancement induced by post-training intrabasolateral amygdala infusions of {beta}-adrenergic or muscarinic agonists requires activation of dopamine receptors: Involvement of right, but not left, basolateral amygdala Learn. Mem., September 1, 2005; 12(5): 527 - 532. [Abstract] [Full Text] [PDF]
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 S. Hamann Sex Differences in the Responses of the Human Amygdala Neuroscientist, August 1, 2005; 11(4): 288 - 293. [Abstract] [PDF]
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H. T. Blair, V. K. Huynh, V. T. Vaz, J. Van, R. R. Patel, A. K. Hiteshi, J. E. Lee, and J. W. Tarpley Unilateral Storage of Fear Memories by the Amygdala J. Neurosci., April 20, 2005; 25(16): 4198 - 4205. [Abstract] [Full Text] [PDF]
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J. G. Pelletier, E. Likhtik, M. Filali, and D. Pare Lasting increases in basolateral amygdala activity after emotional arousal: Implications for facilitated consolidation of emotional memories Learn. Mem., March 1, 2005; 12(2): 96 - 102. [Abstract] [Full Text] [PDF]
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F. Dolcos, K. S. LaBar, and R. Cabeza Remembering one year later: Role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories PNAS, February 15, 2005; 102(7): 2626 - 2631. [Abstract] [Full Text] [PDF]
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