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ORIGINAL ARTICLE
Department of Education and Psychology, 2Dahlem Institute for Neuroimaging of Emotion, Freie Universitt
Berlin, Berlin 14195, Germany, 3Melbourne School of Psychological Sciences, The University of Melbourne,
Parkville, VIC 3010, Australia, and 4Biomedical Imaging, Department of Radiology, Christian-Albrecht University
Kiel, Kiel 24118, Germany
Address correspondence to Dr Carmen Morawetz, Department of Education and Psychology, Freie Universitt Berlin, Habelschwerdter Allee 45, 14195 Berlin,
Germany. Email: carmen.morawetz@fu-berlin.de
Abstract
Reappraisal, the cognitive reevaluation of a potentially emotionally arousing event, has been proposed to be based upon topdown appraisal systems within the prefrontal cortex (PFC). It still remains unclear, however, how different prefrontal regions
interact to control and regulate emotional responses. We used fMRI and dynamic causal modeling (DCM) to characterize the
functional interrelationships among dorsal and ventral PFC regions involved in reappraisal. Specically, we examined the
effective connectivity between the inferior frontal gyrus (IFG), dorsolateral PFC (DLPFC), and other reappraisal-related regions
(supplementary motor area, supramarginal gyrus) during the up- and downregulation of emotions in response to highly
arousing extreme sports lm clips. We found DLPFC to be the central node of the prefrontal emotion regulation network,
strongly interconnected with the IFG. The DCM analysis further revealed excitatory changes of connection strength from the
DLPFC to the IFG and strong inhibitory changes of connection strength between the IFG and DLPFC during reappraisal. These
bidirectional changes in connectivity strength indicate a feedback mechanism by which the IFG may select one out of several
possible goal-appropriate reappraisals held active in working memory (represented in the DLPFC) and inhibits the DLPFC once
the selection process is completed.
Key words: dynamic causal modeling, fMRI, inferior frontal gyrus, reappraisal
Introduction
The cognitive modulation of emotional experience is highly relevant for adaptive social behavior as well as mental and physical
health (Gross and Muoz 1995; Gross and John 2003; Eftekhari
et al. 2009). Reappraisal is the most commonly used and studied
emotion regulation strategy (Gross and John 2003; Ochsner and
Gross 2005; Kalisch 2009; Ochsner et al. 2012; Buhle et al. 2014).
It refers to the cognitive reevaluation of a potentially emotionally
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| Cerebral Cortex
Experimental Procedures
Subjects
Twenty-three right-handed subjects (mean age = 22.95 years, SD
= 3.57 years; 15 females) participated in the study. Handedness
was assessed using the Edinburgh-Handedness Inventory
(Oldeld 1971), and eligibility was assessed using a general health
questionnaire and fMRI safety screening form. Subjects had normal or corrected-to-normal vision and gave written, informed
consent to participate in the study, which was approved by the
ethics committee of the German Psychological Society (DGPs).
dorsolateral prefrontal cortex (DMPFC, DLPFC), which are implicated in selective attention and working memory, thereby promoting the generation of mental representations of affective
states and reappraisal to regulate emotion (Miller 2000; Miller
and Cohen 2001; Curtis and DEsposito 2003; Wager and Smith
2003; Wager et al. 2004; Gazzaley and DEsposito 2007; Ochsner
et al. 2012). The second system is discussed to play a role in
top-down outcome-based appraisal and includes ventromedial
and ventrolateral prefrontal cortex (VMPFC, VLPFC), which are involved in response selection and inhibition, as well as cognitive
control of choice (Aron et al. 2004; Thompson-Schill et al. 2005;
Badre and Wagner 2007; Hare et al. 2009; Ochsner et al. 2012).
In support of the top-down appraisal systems, several studies
demonstrate amygdala-frontal coupling during emotion regulation (Ochsner et al. 2002; Urry et al. 2006; Banks et al. 2007;
Delgado et al. 2008; Kanske et al. 2011). Emotion regulation processes might, however, not necessarily be related to changes in
amygdala activity as previous studies directly contrasting reappraisal strategies with different goal-specicity (Increase and
Decrease) report no modulation of the amygdala (Ochsner, Ray
et al. 2004; Urry et al. 2006; Eippert et al. 2007; Kim and Hamann
2007). Furthermore, meta-analyses demonstrated that the comparison between reappraisal (Increase and Decrease) and an
emotional baseline condition does not yield differences in amygdala activity (Kalisch 2009; Buhle et al. 2014; Kohn et al. 2014).
Thus, emotion regulation processes might be better understood
as a result of the interplay of lateral PFC regions, in line with models which suggest that strategy initiation and application are promoted by these regions (Phillips et al. 2008; Ochsner et al. 2012),
but no study to date has examined changes in effective connectivity between dorsal and ventral prefrontal regions during
reappraisal.
In the present study, participants were asked to up- and
downregulate their emotions while viewing highly arousing extreme sports lm clips in an MRI scanner. We assessed the functional interrelationships among dorsal and ventral PFC regions
involved in reappraisal by combining conventional statistical
parametric mapping (SPM) with dynamic causal modeling
(DCM) of functional magnetic resonance imaging (fMRI) data
(Friston et al. 2003). Previous studies showed that both DLPFC
and VLPFC, including inferior frontal gyrus (IFG), are connected
to temporal and parietal regions (Petrides and Pandya 1999;
Catani et al. 2005; Petrides 2005; Frey et al. 2008; Keller et al.
2009; Geva et al. 2011). Furthermore, DLPFC and VLPFC have
been shown to be interconnected in nonhuman primates (Barbas
and Pandya 1989, 1991; Barbas 2000, 2009; Yeterian et al. 2012)
and in humans (Goulas et al. 2012). Therefore, we hypothesized
that reappraisal, specically the up- and downregulation of emotion, would be driven by the interplay between ventral and dorsal
prefrontal systems, leading to increased reciprocal connectivity
between them.
| 3
Questionnaires
Before and after the fMRI experiment, subjects rated their state
anxiety using the State Trait Anxiety Inventory (STAI) (Spielberger et al. 1970; Laux et al. 1981) to assure that our sample did
not differ from the population average. After the fMRI session,
subjects completed several questionnaires. As the personality
construct of alexithymia encompasses a cluster of characteristics
reecting impaired emotion processing and regulation, we assessed alexithymia with the Toronto Alexithymia Scale (TAS-20)
(Bach et al. 1996). The Sensation Seeking Scale (SSS-V) (Beauducel
et al. 2003) was used to exclude any potential extremely high sensation seekers (not found in our sample).
After the fMRI experiment, we assessed individual differences
in emotion regulation strategies (suppression and reappraisal) by
obtaining self-ratings of emotion experience and expression
using the Emotion Regulation Questionnaire (ERQ) (Gross and
John 2003; Abler 2009). Additionally, subjects rated their ability
to regulate their negative emotions for Increase and Decrease trials
during the fMRI experiment in a separate general questionnaire
on a 7-point scale (1: not successful at all to 7: very successful). Subjects were also asked to rate whether they succeeded
in imagining themselves in the depicted situations in general.
In 2 open questions, subjects were given the opportunity to provide additional feedback regarding the emotion regulation
strategies.
Electrodermal Activity
It has been demonstrated that electrodermal activity (EDA) is
modulated by emotional arousal and emotion regulation (Urry
et al. 2009). We recorded EDA as a measure of affective value of
stimuli using 2 cup electrodes with an internal impedance of
15 k (7 mm) lled with isotonic paste and attached to the proximal phalanges of the index and middle ngers on the left hand.
EDA was acquired at a sampling rate of 5000 Hz using an MRcompatible amplier system (BrainAmp GSR-module, Brain
Products, Gliching, Germany) and constant voltage electrode excitation. During the analysis, the data were down-sampled ofine
to 10 Hz. We applied continuous decomposition analysis to decompose skin-conductance data into continuous tonic and
phasic activity (Benedek and Kaernbach 2010) and averaged
across trials within each condition applying an 8-s time window
using Ledalab Version 3.3.1 (Benedek and Kaernbach 2010). Skinconductance responses (SCRs) were dened as a deection of at
least 0.01 S occurring 18 s after stimulus onset. Only runs
Figure 1. Task Design. Each trial started with an instruction screen of 2 s, displaying a cue for each experimental condition: Red arrow pointing upward symbolized Increase,
video camera indicated Look and green arrow pointing downward indicated Decrease. After the instruction, participants performed the instructed emotion regulation goal
for 8 s while either a neutral or negative lm clip was presented. Subsequently subjects were asked to rate their current emotional state (How negative do you feel?) on a
scale from 1 (weak) to 4 (strong), followed by a xation phase of 48 s.
Morawetz et al.
| Cerebral Cortex
Regions-of-Interest Selection
Prior to the DCM analyses, a conventional second-level fMRI analysis was conducted to determine the ROIs for the DCM analyses.
These group-level analyses were based on random-effects analyses of the single-subject contrast images using the summary
statistic approach. We identied regions, which were involved
in either reappraisal goal (Increase + Decrease) relative to the control condition (Look-Sports) [0.5 0.5 1]) (using a relatively liberal
threshold of P < 0.001 uncorrected and a minimum cluster size
of 50 voxels) in order to obtain regions, which are involved in
reappraisal in general. We specically aimed to identify regions
independent of the emotion regulation strategy used (strategyunspecic). This contrast identied left dorsolateral prefrontal
cortex (DLPFC), left IFG, left supramarginal gyrus (SMG), precentral gyrus, and pre-supplementary motor area ( pre-SMA) (Fig. 2
and Table 3) as ROIs, in line with previous studies describing
the emotion regulation network (Ochsner et al. 2012; Ray and
Zald 2012; Buhle et al. 2014).
To reduce the complexity and size of the model space (Lohmann et al. 2012), we selected the 4 ROIs based on the above contrast (DLPFC, IFG, pre-SMA, and SMG). Previous studies suggested
that precentral gyrus is not crucial for emotion regulation processes but implicated in goal-directed action observation (Grzes
and Decety 2001; Perani et al. 2001; Morin and Grzes 2008); thus,
this region was excluded for the following analyses. The remaining functional ROIs were masked with anatomical ROIs taken
from the WFU Pick Atlas toolbox (version 3.0) (Maldjian et al.
2003) to assure their belonging to a given anatomical region
(DLPFC: x = 53, y = 20, z = 24; IFG: x = 44, y = 25, z = 7; pre-SMA:
x = 6, y = 9, z = 60; SMG: x = 57, y = 45, z = 29). Using this
approach, we aimed to optimize the selection of regions for the
ROIs included in the DCM analysis. Given its general role in visual
stimulus processing, an additional anatomical ROI was determined within the primary visual cortex (BA 17, V1), using a
sphere of 10 mm around the central coordinates of V1 according
to the WFU Pick Atlas (x = 8, y = 85, z = 3).
Morawetz et al.
| 5
Figure 2. Emotion regulation-related activation. Emotion Regulation (Increase + Decrease) versus Look (P < 0.001 uncorrected, k = 50). Left dorsolateral prefrontal cortex
(DLPFC), left inferior frontal gyrus (IFG), left supramarginal gyrus (SMG), and left supplementary motor area (SMA) were used as regions of interest for the subsequent
DCM analysis (highlighted).
to the model space one tests. The different models can be compared with all other models to determine which model best predicts the data using a Bayesian Model Selection (BMS) scheme
(Penny et al. 2004). Multiple models can further be grouped into
families, which share a common element of interest and can be
compared (Penny et al. 2010).
After dening the 5 ROIs, the principal eigenvariate time series was extracted from each ROI within a 6-mm radius sphere of
the local maxima on a single-subject level and adjusted to the
F-contrast (Increase, Decrease, Look-Sports, Look-Neutral) of each
subject. Based on these time courses, DCM, as implemented in
DCM10 (SPM8), was used to model the effective connectivity between these regions. For the DCM analysis, we recombined the
regressors of the univariate analysis to extract the time courses:
1) Film Clips (all experimental conditions: Increase, Decrease,
Look-Sports, Look-Neutral), 2) Sports Film Clips (all sports lm
clips: Increase, Decrease, Look-Sports), and 3) Emotion Regulation (reappraisal conditions: Increase, Decrease).
| Cerebral Cortex
(SMG), dorsolateral prefrontal cortex (DLPFC), supplementary motor area (SMA), and inferior frontal gyrus (IFG) only in the left hemisphere. All models within one
family have the same endogenous connections. Modulated changes in connectivity by emotion regulation are shown with thicker arrows. Models are arranged in
respect to their complexity: Models of the rst row (01, 02, 10, 11) include one modulatory effect; models of the second and third row (0308, 1217) include 2 and 3
modulatory effects, respectively; models of the last row (09 and 18) represent the most complex models with 4 modulatory effects. Driving input of all conditions
(Increase, Decrease, Look-Sports, Look-Neutral) enters V1 in all models. A The 9 models that constitute the rst family with DLPFC (red) as central node. B The 9
models that constitute the second family with IFG (blue) as central node.
Table 1 Questionnaires
Questionnaire
STAI ( pre-experiment)
STAI ( postexperiment)
TAS-20
Reappraisal (ERQ)
SSS
Female (n = 15)
Male (n = 7)
Total (n = 22)
SD
PA
PA SD
SD
PA
PA SD
36.73
38.23
41.93
2.95
22.00
6.48
9.63
10.09
0.76
4.91
32.57
33.85
43.45
4.24
16.9
8.01
13.04
9.8
0.9
5.5
35.40
36.70
41.00
2.61
22.71
7.09
10.81
12.20
1.51
5.58
36
10
47.19
4.07
19.9
10.3
1.2
6.6
SD
41.63
2.84
22.22
10.52
1.03
5.01
PA
PA SD
STAI, State Trait Anxiety Inventory; TAS-20, Toronto Alexithymia Scale-20; ERQ, Emotion Regulation Questionnaire; SSS, Sensation Seeking Questionnaire; M, mean; SD,
standard deviation; PA, population average; PA SD, standard deviation of population average.
PA for STAI: Spielberger et al. (1970); PA for TAS-20: Parker et al. (1993); PA for ERQ: Abler (2009); PA for SSS: Beauducel et al. (2003).
Random-Effects BMS
For each subject, all 18 models had the same endogenous connections and driving input within one family but differed in respect to the modulatory effects (Fig. 3, bold arrows). In a rst
step, we tested which family of models has the higher likelihood
using random-effect BMS at the family level as implemented in
SPM8. We computed the evidence of each family of models,
Figure 3. Model specication. Illustration of the 18 different models estimated and compared here. The sources comprising the models were V1, supramarginal gyrus
Morawetz et al.
| 7
Results
Behavioral Results
Emotion Induction
To assess whether the stimuli induced the desired emotion, subjects rated all previously seen lm clips on valence and arousal in
a postscan session. Subjects rated the extreme sport lm clips as
more arousing (arousal: sport lm clips: M = 5.07, SE = 0.25;
neutral clips: M = 2.40 0.29; t (22) = 8.55, P < 0.001; 1 = calm to
9 = highly arousing) and less positive (valence: sports lm clips:
M = 6.04 0.23; neutral clips: M = 7.30 0.26; t (22) = 4.70, P < 0.001;
1 = negative to 9 = positive) than the neutral lm clips.
Skin-conductance data provided additional support for the
success of the emotion induction by indicating an increase or decrease in arousal (Fig. 4A): In both Increase (t (22) = 3.87, P < 0.001)
and Decrease (t (22) = 3.00, P < 0.01) conditions, SCR amplitudes
were higher compared with the control condition (Look-Neutral).
Increasing (t (22) = 1.68, P = 0.10) and decreasing (t (22) = 0.76, P = 0.45)
emotion was not signicantly different from the Look-Sports condition. The difference of SCR amplitudes during the emotion
regulation phase bordered signicance and were higher for the
Increase than for the Decrease condition (t (22) = 2.08, P = 0.05).
SCRs in Look-Sports were signicantly increased compared with
Look-Neutral (t (22) = 3.85, P = 0.001).
Emotion Regulation
Analysis of the emotional state ratings (ranging from 1 = not at all
negative to 4 = extremely negative) after each trial in the scanner
revealed a signicant main effect of task condition (F1,22 = 70.95,
P < 0.001) (Fig. 4B). Signicantly greater negative affect was reported for the sports clips (M = 1.81 0.45) compared with the
neutral lm clips (M = 1.25 0.22) in the Look condition (t (22) =
7.36, P < 0.001), conrming that sports clips induced relatively
more negative affective responses. Comparisons between task
conditions showed that the reappraisal tasks signicantly
differed from Look conditions, conrming that the reappraisal
instruction resulted in successful increase (M = 2.50 0.52)
and decrease (M = 1.71 0.54) of negative affect, respectively
(Increase > Look-Sports: t (22) = 8.64, P < 0.001; Increase > LookNeutral: t (22) = 11.65, P < 0.001; Decrease > Look-Sports: t (22) =
1.98, P = 0.06; Decrease > Look-Neutral: t (22) = 4.95, P < 0.001).
Furthermore, we tested for effectiveness of emotion regulation ( percent effective trials), which was above average for Increase (M = 75%, SD = 21.99, t (22) = 5.54, P < 0.001) and Decrease
(M = 72%, SD = 20.97, t (22) = 5.12, P < 0.001). There was no signicant difference in effectiveness between the 2 regulation conditions (t (22) = 0.425, P = 0.68).
fMRI Results
Emotion Induction
First, we contrasted activation during exposure to all extreme
sport clips (Increase, Decrease, Look-Sports) with the neutral lm
clips to search for neural correlates of the emotional effects. Increased activity was observed in a widespread network of regions
including middle temporal gyrus, SMG, IFG, cingulate cortex, and
fusiform gyrus (Table 2).
Emotion Regulation
Next, we investigated activity changes due to emotion regulation.
For this, we contrasted both emotion regulation goals (Increase,
Decrease) to the control condition (Look-Sports). This analysis revealed that the SMA, SMG, IFG, DLPFC, and precentral gyrus
were activated during reappraisal regardless of the reappraisal
goal (Fig. 2 and Table 3). Based on our a priori hypotheses and previous ndings that some of these regions will not be directly involved in emotion regulation but rather have supportive
Confound Control
A battery of questionnaires (see Materials and Methods) was
administered. Our sample did not differ from the reported population averages (PA), that is, differed less than 1 standard deviation (SD) from the mean on state anxiety (using the STAI, Laux
et al. 1981), alexithymia (using TAS-20, Parker et al. 2003), sensation seeking (using the SSS, Beauducel et al. 2003), and individual
differences in general emotion regulation strategies (reappraisal
and suppression) (using the ERQ, Abler 2009) (Table 1).
After scanning, subjects rated their ability to regulate their
emotions during the study (1 = very bad to 7 = very good) as
above average for Increase (M = 4.65, SD = 0.27, t (18) = 3.92, P < 0.01)
and Decrease (M = 4.75, SD = 0.29, t (18) = 3.86, P < 0.01), and for
their ability to vividly put themselves into the depicted situation
(M = 5.05, SD = 0.99, t (18) = 6.53, P < 0.001). When asked about their
emotion regulation strategies after the fMRI session, more than
half of all subjects explicitly stated that they used inner speech
to regulate their emotions (n = 13).
| Cerebral Cortex
DCM Results
We constructed 18 models, separated in 2 families, each of which
assumed either the DLPFC or the IFG as the central node (see Materials and Methods). First, the winning family across all subjects
was identied using random-effects BMS at the family level to
determine the optimal intrinsic connections and modulations
of emotion regulation. The results revealed that family #01,
Table 4 Parameters of the model with the best t (model 6), including
intrinsic connections, modulation of intrinsic connections, and
driving inputs (family #01)
Region
Side
Size
Z-score
R
R
L
R
R
L
R
L
R
L
R
L
R
48
57
60
6
42
48
45
6
12
15
18
30
27
61
37
40
19
23
20
46
28
76
76
49
40
64
13
25
25
43
10
8
20
5
40
37
50
38
29
471
198
629
3138
224
165
20
182
76
34
80
30
14
6.90
6.77
6.74
6.50
5.57
4.98
4.87
5.16
5.46
4.70
4.90
4.80
4.61
Mean (Hz)
Cingulate cortex
Inferior frontal gyrus
Fusiform gyrus
Thalamus
Cuneus
Cerebellum
SD (Hz)
P (corr.)
0.03
0.56
0.95
0.73
0.67
0.65
6.19
4.25
4.08
5.73
2.33
4.45
<0.001
<0.001
<0.001
<0.001
n.s.
<0.001
1.05
0.81
0.73
1.07
3.06
3.67
n.s.
0.005
0.001
0.41
7.33
<0.001
L, left; R, right.
P < 0.05; FWE corrected, k = 10.
Table 3 Regions activated by emotion regulation (Increase and Decrease) relative to Look-Sports
Region
Side
Size
Z-score
R
L
L
L
L
3
60
48
42
18
8
46
23
2
59
67
28
8
52
31
628
114
297
115
56
5.83
4.93
4.80
4.15
3.79
L, left; R, right.
P < 0.001; uncorrected, k = 50.
Morawetz et al.
| 9
represent context-dependent changes in coupling between regions induced by emotion regulation. A graphic illustration of
these connectivity changes for model 6 due to emotion regulation processes is shown in Figure 8. Reappraisal reduced the
effective connectivity between the DLPFC and IFG in both directions. However, given the initial positive intrinsic coupling between the DLPFC and IFG, the negative modulatory inuence
was not sufcient to reverse the sign of DLPFC-IFG coupling, as
evident from the persisting positive total connectivity. On the
other hand, the IFG effectively inhibited the DLPFC during emotion regulation, as reected by the sum of the posterior intrinsic
parameters and modulation parameters yielding a net modulation that became more negative.
Discussion
Figure 6. ROI analysis of the left and right amygdala. Amygdala responses as
function of task conditions. Error bars represent standard error of the mean.
Figure 5. ROI analysis of the (A) left dorsolateral prefrontal cortex (DLPFC), (B) left inferior frontal gyrus (IFG), (C) left supplementary motor area (SMA), and (D) left
supramarginal gyrus (SMG). Responses as function of task conditions. Error bars represent standard error of the mean.
10
| Cerebral Cortex
Figure 7. BMS results. Exceedance probability for all models of family #01. Notably, the winning model 6 outperformed the more complex model 9. Both are illustrated in
Morawetz et al.
| 11
arrows represent connectivity strength in Hz (only signicant results are depicted). (A) Intrinsic connectivity (black arrows). (B) Modulation of connectivity by emotion
regulation (ER). BMS results and SD are shown.
Figure 8. Graphic illustration of model 6, which was found to have the best t (Table 3). Driving input (not shown graphically) enters through V1. The values under the
12
| Cerebral Cortex
Supplementary Material
Supplementary material can be found at: http://www.cercor.oxfordjournals.org/
Funding
This work was supported by Excellence Initiative of the German
Federal Ministry of Education and Research Deutsche Forschungsgemeinschaft Grant EXC 302.
Notes
We thank Danny Strasser (www.danny-strasser.de), Jrgen Brath
(www.gojump.de), and Red Bull Media House (www.redbull.com)
for providing the lm clips. Conict of Interest: None declared.
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