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International Journal of Psychophysiology 79 (2011) 364–370

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International Journal of Psychophysiology


j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / i j p s yc h o

Anger and cardiovascular startle reactivity in normotensive young males


Steffen Richter a,⁎, Hans-Christian Deter b, Miriam Rudat b, Hartmut Schächinger a,
Frank Zimmermann-Viehoff b, Cora Weber b
a
University of Trier, Institute of Psychobiology, Department of Clinical Physiology, Trier, Germany
b
Department of Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Campus Benjamin Franklin, Berlin, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Anger has been implicated in the etiology of hypertensive disease. Trait anger has been linked to enhanced
Received 18 June 2010 cardiovascular responsiveness. However, whether this association reflects differences in context appraisal or a
Received in revised form 13 December 2010 general hyper-reactivity of the cardiovascular system remains unclear. We studied the cardiovascular
Accepted 15 December 2010
response to acoustic startle probes in 76 healthy Caucasian males in different affective contices (pleasant,
Available online 22 December 2010
neutral, and unpleasant). All participants completed the State-Trait-Anger-Expression-Inventory (STAXI) by
Keywords:
Spielberger and the results were analysed with stepwise regression analysis according to the anger scores and
Anger traditional risk factors for hypertension. Our study reveals differential modulation of the cardiovascular
Startle reflex response to startle stimuli by affective pictures in the dimensions “valence” for heart rate and “arousal” for
Cardiovascular reactivity blood pressure. Anger-in was identified as the most important determinant for blood pressure responses in
Affective modulation unpleasant context, while anger-out was associated with less cardiovascular activation in neutral context.
This is the first study that relates trait anger to cardiovascular reactivity and affective reflex modulation in
normotensive subjects. We could demonstrate an interaction of affective context and trait anger for
cardiovascular (hyper-)reactivity. Increased cardiovascular reactivity for higher scores of anger-in in
unpleasant context may indicate enhanced sympathetic reactivity and constitute a risk factor for the
development of essential hypertension.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction the arteries (Schlaich et al., 2004). Furthermore, enhanced sympa-


thetic activity can promote later hypertension without preceding
The prevalence of hypertension has been rising continuously in blood pressure elevations. Enhanced sympathetic activity unfolds
modern society. The contribution of psychosocial factors such as deleterious effects on the cardiovascular system (Mancia et al., 1999),
suppressed anger has been suggested early in hypertension research promoting media sclerosis and heightened vascular resistance
(Alexander, 1939). Anger has repeatedly been linked with the (Ferriss, 1978; Markovitz et al., 1993).
etiology of essential hypertension (Deter et al., 2001; Dimsdale However, little is known about the affective modulation of blood
et al., 1986). A recent review found a consistent association of trait pressure responsiveness and the relationship between anger and
anger and ambulatory blood pressure (Schum et al., 2003). It has been cardiovascular reactivity in a healthy population. Especially “anger-
hypothesized that trait anger causes increased physiological arousal in”, i.e. anger directed towards the own person, held or suppressed
by interacting with situational factors (Jorgensen et al., 1996). In line anger feelings, and “anger out”, i.e. overtly and directly expressed
with this, trait anger has been linked to enhanced cardiovascular anger towards other persons or environmental objects (Forgays et al.,
reactivity (Bongard et al., 1998; Vogele et al., 1997) and increased 1997) appear to be positively correlated with resting systolic blood
sympathetic activity (McCraty et al., 1995). Indeed, a functional blood pressure (Bongard and al'Absi, 2005; Igna et al., 2009; Vogele and
pressure rise in stressful situations can precede a permanently Steptoe, 1992). Negative correlations with resting diastolic blood
elevated blood pressure that is solidified by structural changes of pressure have been reported (Schum et al., 2003; Spicer and
Chamberlain, 1996), but contradictory findings exist (Holroyd and
Gorkin, 1983; Igna et al., 2009; Shapiro et al., 1997). “Anger-in” is also
Abbreviations: ECG, electrocardiogram; EMG, electromyogram; BMI, body mass positively correlated with systolic blood pressure reactivity during
index; SU, standardized units; mmHg, millimeter mercury; bpm, beats per minute; stressful tasks (Burns, 1995; Holroyd and Gorkin, 1983; Mills and
IAPS, International Affective Picture System; STAXI, State-Trait-Anger-Expression- Dimsdale, 1993; Vogele and Steptoe, 1992), while mixed results exist
Inventory; SAM, Self-Assessment Manikin questionnaire.
⁎ Corresponding author. University of Trier, Department of Psychobiology, Johanniterufer
for “anger-out”. Although consistently associated with higher systolic
15, 54290 Trier, Germany. Tel.: +49 6512013661; fax: +49 6512013737. blood pressure at rest, both positive (Burns, 1995; Faber and Burns,
E-mail address: richters@uni-trier.de (S. Richter). 1996; Vogele and Steptoe, 1992) and negative (Haeri et al., 1996;

0167-8760/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijpsycho.2010.12.004
S. Richter et al. / International Journal of Psychophysiology 79 (2011) 364–370 365

Holroyd and Gorkin, 1983; Vogele and Steptoe, 1992) correlations Ewart and Kolodner, 1994; Shapiro et al., 1995), hereditary factors
with systolic blood pressure reactivity to stress have been reported. (Lawler et al., 1998; Shapiro et al., 1995; Vogele and Steptoe, 1992),
Assessing cardiovascular stress reactivity in subjects differing in and ethnic background (Durel et al., 1989; Ewart and Kolodner, 1994;
trait anger may potentially be biased by differences in task perception. Shapiro et al., 1995). To control for these factors, only healthy
The startle reflex represents a valuable tool for the investigation of Caucasian males were included into the study sample and family
cardiovascular responses to external stimulation and the modulation history of hypertension was assessed during the medical screening.
of such responses by affective context. In contrast to other stimuli that We included 80 volunteers. Four of these had to be excluded from
are commonly used to elicit a cardiovascular reaction (e.g. math task, statistical analysis. Two participants demonstrated repeatedly elevat-
cold pressor, interview stress, etc.), the startle reflex is brainstem ed blood pressure in the experimental setting (N160 mmHg) and two
relayed and therefore does not require higher cognitive processing of others had to be excluded due to technical difficulties during the
the eliciting stimulus itself. recordings. Applicants with known cardiovascular disease, other
The startle reflex is part of the defensive reflex system and acute or chronic illnesses, smokers, and shift workers were excluded.
accompanied by a cardiovascular response consisting of a rise in heart All participants underwent routine physical examination. Participants
rate and blood pressure (Girard et al., 2001; Holand et al., 1999a; had a mean age of 25.5 ± 2.6 years and a BMI of 22.8 ± 2.3 kg/m².
Holand et al., 1999b). The amplitude of the motor response (as Mean systolic blood pressure on physical examination prior to the test
measured by electromyogram of the musculus orbicularis oculi) is was 110 ± 7.8 mmHg, mean diastolic blood pressure 55.8 ± 5 mmHg,
enhanced in negative affective context (match condition: when the and mean heart rate 57.7 ± 8.6 beats per minute. Mean values for
context matches the aversive character of the reflex) and diminished physical activity (subjective rating scale, see below) were 1.9 ± .78
in positive affective context (mismatch condition). The same pattern arbitrary units. The study was approved by the local ethics committee
of modulation has been found for heart rate responses to startle of the hospital (University Hospital Benjamin Franklin, Berlin,
stimuli (Bradley et al., 1990; Cook et al., 1992; Gautier and Cook, Germany). All participants gave written consent before being
1997). Although some studies reported inconsistent results for included and were free to leave the study at any point.
reactions in pleasant context (Bradley and Lang, 2000; Sanchez
et al., 2002), these studies demonstrate an affective modulation of the
heart rate reaction that is elicited by the brainstem mediated startle 2.2. Stimulus material
reflex. The affective modulation of the blood pressure response to
startle stimuli has, to our knowledge, not been investigated yet, but The affective pictures were selected from the International
there is evidence that enhanced affective startle modulation is Affective Picture System (IAPS) (Lang et al., 1988). The IAPS is a
associated with generally enhanced blood pressure reactivity. Gautier well established method for affective stimulation. The system
and Cook found enhanced affective startle modulation in individuals contains a large number of slides that have been rated for valence
with enhanced blood pressure response to mental stress (Gautier and (i.e. the emotion elicited by the slide ranging from “unpleasant = 0” to
Cook, 1997). Also, enhanced affective startle modulation has been “pleasant = 9”) and arousal (i.e. how much arousal is elicited by the
linked to physiological characteristics such as salt sensitivity and slide ranging from “low = 0” to “high = 9”). Pleasant (e.g. nature
psychological states or traits such as anxiety, irritability, and anger scenes, erotic pictures), neutral (e.g. household items, colored
(Buchholz et al., 2001) that in turn are considered risk factors for textures), and unpleasant pictures (e.g. fierce animals, mutilation
hypertension. pictures) were presented.1 Slides were selected to have equal ratings
In this study, we investigated the affective modulation of heart rate for valence within each category (pleasant: 7.6 (sd = 0.54); unpleas-
and blood pressure responses to startle stimuli in normotensive ant: 2.8 (sd = 0.65); neutral: 5.09 (sd = 0.28)) based on the original
subjects. We furthermore investigated how anger affects the IAPS ratings by Lang et al. (1988). Positive and negative slides were
cardiovascular response to startle stimuli. Trait "anger expression" selected to have comparable ratings for arousal (5.84 (sd = 1.05) and
(with the dimensions “anger-out" and “anger-in”) as well as trait 5.93 (sd = 0.92), respectively). Neutral slides are generally rated as
“anger control” were assessed with the German version of the State- less arousing (3.22 (sd = 1.0)). The startle stimuli consisted of 95 dB
Trait-Anger-Expression-Inventory (STAXI). Pictures of different emo- white noise of 50 milliseconds duration and instantaneous rise time
tional content (valence) and acoustic startle stimuli were presented to (noise generator provided by Dr I. Curio, Medizinelektronik, Bonn,
the participants while startle magnitude, heart rate, and blood Germany).
pressure were recorded. Self-ratings of the visual stimuli were
obtained to control for differences in perceived affective stimulation
2.3. Questionnaires
and correlated with anger scores.
We hypothesized that the startle reflex would be accompanied by
All participants completed a questionnaire assessing traditional
a significant cardiovascular response (i.e. an increase of heart rate and
risk factors for hypertensive disease, i.e. family history of hyperten-
blood pressure) modulated by affective context (i.e. an increase in
sion, age, BMI, and physical activity. Participants were categorized as
unpleasant context, and a decrease in pleasant context). We
positive for “family history of hypertension” if at least one first grade
furthermore assumed that trait anger would have a significant effect
relative had a history of clinically relevant hypertensive disease.
on the cardiovascular response to startle stimuli. We hypothesized
Physical activity was assessed on a subjective rating scale ranging
that this effect would be independent of affective context in case of a
from 0 (no physical activity) to 3 (high level of physical activity, e.g.
general hyper-reactivity of the cardiovascular system, or depending
regular endurance training).
on affective context in case of an underlying difference in context
appraisal. 1
Complete list of IAPS-pictures used in the experiment: Original ratings for valence and
arousal are presented in brackets (valence/arousal). Pictures in brackets were not included
2. Methods into statistical analysis, because they were followed or preceded by another startle in too
close temporal relationship. Pleasant pictures: 1710 (8.02/5.53), 8200 (7.15/6.33), 7580
2.1. Participants (7.4/5.08), 4250 (8.39/7.02), 1750 (7.89/4.21), 7230 (7.42/5.81), 2160 (6.87/5.31), 4180
(8.21/7.43), 1600 (6.95/4.08). Unpleasant pictures: 6360 (2.63/5.8), 6230 (2.73/7.1), 2800
(2.31/4.94), 6540 (2.53/6.51), 1120 (4.73/6.6), 9140 (2.56/4.9), 1300 (4.06/6.9), 2120
We recruited healthy male volunteers for the study via advertise- (3.65/4.93), 3030 (2.31/6.39). Neutral pictures: 7550 (5.39/4.48), 7010 (4.95/1.55), 7130
ment on university black boards. The relationship between trait anger (4.79/3.54), 9070 (4.88/3.51), 7830 (5.31/4.40), 7090 (4.95/2.30), 7100 (5.29/3.08), 2190
and blood pressure may be affected by gender (Durel et al., 1989; (4.73/2.27), 7190 (5.5/3.89)
366 S. Richter et al. / International Journal of Psychophysiology 79 (2011) 364–370

Furthermore, all participants completed the German version of the response onset. EMG data were z-transformed for further analysis.
State-Trait-Anger-Expression-Inventory (STAXI (Spielberger, 1988); Because z-transformation matches all participants in response
German translation by Schwenkmezger and Hodapp (1991). The magnitude and may therefore preclude the detection of differences
STAXI measures trait anger expression including the dimensions due to trait anger, an additional correlation analysis of absolute (non-
“anger-out”, that is anger directed towards the outside world (objects transformed) EMG data with trait anger scores was performed. ECG
or persons) and “anger-in”, that is anger directed towards the own and blood pressure were offline controlled for artifacts by visual
person or suppressed anger, as well as the trait “anger control”, a artifact control. The beat-to-beat values were automatically adjusted
measure for a successful and healthy control of anger. Subjective to values per second by Turbo Pascal based software, and a period of
ratings of arousal and valence induced by each picture were assessed 10 s after the startle stimulus was included in the analysis. All further
by the Self-Assessment Manikin questionnaire (SAM) (Bradley and analysis was based on second-by-second data.
Lang, 1994) immediately after the experiment. Statistical analysis was performed by SPSS+ version 15 (SPSS Inc.,
Chicago, Illinois, USA). Statistical analysis of startle EMG responses and
2.4. Physiological data valence and arousal ratings of visual stimuli were done by an ANOVA of
repeated measures design with the within subjects factor “affective
During the startle trial heart rate was continuously recorded by context” (“neutral”, “pleasant”, and “unpleasant”). Subjective valence
ECG with standard Ag/AgCl electrodes in lead II configuration. Blood and arousal ratings of visual stimuli were then correlated with anger
pressure was continuously recorded by a Finapres device (Ohmeda, scores by bivariate correlation analysis. Statistical significance of the
USA). Electromyographic recording of muscular activity from the cardiovascular response and its affective modulation were tested using a
musculus orbicularis oculi was obtained as index of reflex strength. All 3 × 10 ANOVA of repeated measures design with the within-subjects
raw signals were recorded at 1000 Hz by DOS software (Turbolab, factors “affective context” and “response” (cardiovascular response over
Stemmer PC-Systeme, Puchheim, Germany). Signals were amplified 10 s after the startle stimulus). Analysis of contrasts (Bonferroni
(TG424, Schwarzer, Munich, Germany) and in addition to the adjusted pairwise comparisons) was calculated for all ANOVAs. The
electronically recorded data recorded on paper by a polygraph impact of anger scores (anger-in, anger-out, and anger-control) and
(UniEDAipt UD210, Schwarzer, Munich, Germany). The electromyo- classical risk factors for hypertension (age, BMI, physical activity and
graphic data were amplified and rectified using a root-mean square family history of hypertension) on the maximal cardiovascular response
rectifier and integrator (time constant, 10 ms). after startle stimuli in different affective context was tested with a
stepwise regression analysis (linear regression model). All predictor
2.5. Study protocol variables were processed in a separate model for each valence category
and entered (or excluded) according to their statistical contribution in
Participants presented at the laboratory at a separate day to explaining the variance in the cardiovascular response. Collinearity
familiarize with the location, for medical screening and resting blood diagnostics were calculated for all regression models. Results were
pressure measurement. To obtain reliable blood pressure measure- Greenhouse-Geisser corrected, whenever indicated by Mauchly's test of
ments, blood pressure was measured in a supine position every minute sphericity. Values of p b 0.05 were considered statistically significant.
over 1 h with a Dinamap device (Dinamap, Criticon, Tampa, USA). The
mean of these measurements was taken as resting blood pressure. 3. Results
On the experimental day, participants were welcomed and seated in
a quiet room with dim light. Electrodes for the ECG and EMG as well as 3.1. Questionnaires
the blood pressure monitor were attached. A series of 42 pictures from
the International Affective Picture System (IAPS) (Lang et al., 1988) Subjective ratings of the visual stimuli were significantly different for
was presented on a 19-inch standard PC screen at a distance of valence (F(2,150) = 815.18, p b .001, η² = .916) and arousal (F(2,150) =
approximately 30 in. The only instruction given to the participants was 247.24, p b .001, η² = .767). Analysis of contrast demonstrated that
to view the pictures during the whole presentation period. The picture valence ratings for pleasant (7.05 ± .71 AU) and unpleasant (2.54 ±
sequence was divided into three blocks of 14 pictures each. In each block .76 AU) pictures were significantly different from ratings for neutral
one picture of each valence was missing, to enhance the unpredictability (5.43 ± .63 AU) pictures (pb .001 and p b .001) and from one another
of the valence category for the last pictures. Thus, 5 pictures of two (pb .001). Unpleasant (5.23± 1.17 AU) pictures were rated as most
categories and 4 pictures of the remaining category were presented arousing, with significant differences to pleasant (3.99 ± 1.22 AU) and
during each block in semi-randomized counterbalanced order. The neutral (2.42 ± 1.05 AU) pictures (p b .001 and p b .001). Pleasant
blocks were presented in randomized order. Each picture was presented pictures were rated as significantly more arousing than neutral pictures
for 6 s, followed by 14 s of dark screen. Startle probes were delivered (pb .001).
binaurally over monophonic headphones. Startle probes were pre- Anger-control was positively correlated with anger-in (r = .30,
sented during three pictures of each valence category in each block p = .008) and negatively correlated with anger-out (r = −.47,
(65% of the pictures) and three times in the dark period (21.4% of all p b .001). Anger scores were not significantly correlated with classical
dark periods). The probe onset varied from 2 to 5 s after picture onset risk factors for hypertension, i.e. age, BMI, physical activity or family
(or offset for startle probes in the dark period). history for hypertension. Anger-out scores were positively correlated
with valence ratings of pleasant pictures (r = .23, p = .043), while anger-
2.6. Data reduction and analysis in scores were positively correlated with arousal ratings of unpleasant
pictures (r= .24, p = .034), but not with valence ratings. BMI correlated
Questionnaire data were manually transferred into SPSS for positively with positive valence ratings (r = .25, p = .029). Family
further analysis. Heart rate was derived from ECG data by calculating history of hypertension correlated positively with neutral (r=.32,
the R to R distances by Turbo Pascal based software. The heart rate and p = .005), but negatively with positive ratings (r =−.29, p = .010).
blood pressure responses were calculated as change from the values
immediately before the respective startle stimulus. Blink magnitude 3.2. Startle EMG responses
was calculated as the maximum of ms 20 to 150 following the startle
stimulus, expressed as change from the median of 50 ms before the Startle eye blink magnitude was enhanced in unpleasant context
upstroke of the blink response. EMG data were excluded if they and diminished in pleasant context (F(2, 150) = 13.55, p b .001,
fluctuated by more than 30% of the amplitude within 50 ms before η² = .153), although analysis of contrasts revealed significant
S. Richter et al. / International Journal of Psychophysiology 79 (2011) 364–370 367

differences for pleasant versus neutral context only (p b .001). Mean


z-standardized EMG responses were − 0.04 ± .4 standardized units
(SU) in neutral, − 0.23 ± .41 SU in pleasant and 0.01 ± .49 SU in
unpleasant context. Importantly, EMG responses to startle stimuli
(both z-transformed and absolute values) were not significantly
correlated to any trait anger dimension in any affective context,
suggesting similar reflex magnitudes.

3.3. Cardiovascular responses to startle stimuli

We observed a significant increase of heart rate (F(9,675) = 6.52,


p b .001, η² = .080), systolic (F(9,675) = 22.97, p b .001, η² = .234) and
diastolic (F(9,675) = 14.15, p b .001, η² = .159) blood pressure after
the startle stimuli (main effect “response”). Heart rate responses were
increased by unpleasant context (maximum 3.1 ± 1.9 bpm) and
decreased by pleasant context (maximum 2.3 ± 2.1 bpm) as com-
pared to neutral context (maximum 2.7 ± 2.0 bpm) (F(2,150) = 7.02,
p = .001, η² = .086; main effect “affective context”). This pattern of
modulation paralleled the EMG responses. Similar to EMG responses,
analysis of contrasts revealed significant differences for pleasant
versus neutral context only (p = 0.035).
Systolic blood pressure responses were increased by unpleasant
(maximum 3.3 ± 3.4 mmHg) as well as pleasant (maximum 3.6 ±
2.9 mmHg) context, compared to neutral context (maximum 2.2 ±
2.4 mmHg) (F(2,150) = 7.06, p = .001, η² = .086; main effect “affective Fig. 1. Change of heart rate during 10 s after the startle stimulus. Lines represent change
of heart rate (mean of all participants, n = 76). Different lines represent different
context”). Analysis of contrasts revealed significant differences between
affective contices, error bars represent 95% confidence interval of mean.
the responses in unpleasant versus neutral (p= 0.037) and pleasant
versus neutral context (p= 0.001). The same pattern of modulation was
observed for diastolic blood pressure, with an increase in unpleasant a positive correlation with family history of hypertension (ß = .218,
(maximum 1.9 ± 1.6 mmHg) and pleasant context (maximum 2.0 ± t = 2.080, p = .041) and age (ß = .214, t = 2.049, p = .044) in
1.7 mmHg), compared to neutral context (maximum 1.5 ± 1.4 mmHg) unpleasant context. Although diastolic blood pressure responses
(F(2,150) = 3.75, p = .026, η² = .048; main effect “affective context”). were best predicted by anger-out in neutral and anger-in in
Analysis of contrasts revealed a significant difference of responses in unpleasant context, we also observed a negative correlation with
unpleasant versus neutral context (p= 0.037). Heart rate and blood physical activity (ß = −.220, t = −2.042, p = .045) in neutral and
pressure responses in different affective contices are summarized in with BMI (ß = −.237, t = −2.202, p = .031) in unpleasant context.
Figs. 1, 2 and 3.
3.6. Impact of affective pictures without startle stimulus presentation
3.4. Impact of trait anger on the cardiovascular response to startle
stimuli Since the presentation of affective pictures may itself impact on
heart rate and blood pressure, we analyzed the response to pictures
Stepwise regression analysis revealed that in neutral context heart
rate responsiveness was negatively correlated with anger-out (ß=
−.235, t = −2.127, p = .037), while systolic blood pressure respon-
siveness was positively correlated with anger-in (ß= .314, t = 3.006,
p = .004). For diastolic blood pressure a negative correlation with
anger-out (ß= −.312, t = −2.897, p = .005) was found in neutral
context. Trait anger did not correlate with heart rate responsiveness in
pleasant or unpleasant context. However, systolic blood pressure
responsiveness was positively correlated with anger-in in unpleasant
(ß= .306, t = 2.760, p = .007) but not in pleasant context. Also diastolic
blood pressure responses were positively correlated with anger-in
(ß= .348, t = 3.233, p = .002) in unpleasant but not in pleasant context
(Figs. 4 and 5).

3.5. Impact of other risk factors for hypertensive disease

Stepwise regression analysis furthermore revealed that heart rate


responsiveness in all affective contices was influenced by physical
activity (ß = −.231, t = −2.088, p = .040 for neutral, ß = −.307, t =
−2.779, p = .007 for pleasant and ß = −.303, t = −2.734, p = .008 for
unpleasant context), with smaller heart rate responses for higher
physical activity. Although anger-in had the highest predictive value
for systolic blood pressure reactivity in all affective contices, we also
Fig. 2. Change of systolic blood pressure during 10 s after the startle stimulus. Lines
found a negative correlation with physical activity (ß = −.253, t = represent change of systolic blood pressure (mean of all participants, n = 76). Different
−2.292, p = .025) in neutral context. Furthermore, there was a lines represent different affective contices, error bars represent 95% confidence interval
negative correlation with BMI (ß = −.264, t = −2.508, p = .014) and of mean.
368 S. Richter et al. / International Journal of Psychophysiology 79 (2011) 364–370

Fig. 4. Correlation of maximum systolic blood pressure responses to startle stimuli


during unpleasant context and anger-in (mean of all participants, n = 76).

Fig. 3. Change of diastolic blood pressure during 10 s after the startle stimulus. Lines dimension of the foreground stimuli) that was found for EMG and
represent change of diastolic blood pressure (mean of all participants, n = 76). Different heart rate responses (Bradley and Lang, 2000; Lang et al., 1990; Miller
lines represent different affective contices, error bars represent 95% confidence interval
et al., 2002; Vanman et al., 1996), we found the blood pressure
of mean.
responses enhanced in both pleasant and unpleasant context. Both
pleasant and unpleasant pictures were rated as more arousing than
neutral pictures, as previously described (Lang et al., 1988). We
without startle stimulus presentation. A 3 × 4 ANOVA of repeated may therefore assume that the observed pattern reflects a modulation
measures design was conducted with the within-subjects factors by the arousal inherent in the foreground pictures. An influence of
“affective context” and “response” (cardiovascular response over the arousal on the startle reflex has been described before (Sanchez-
4 s during which startle stimuli were presented, i.e. second 2 to 5 after Navarro et al., 2008), but it has never been demonstrated for the
picture onset). No significant impact of affective context was found for cardiovascular response to startle stimuli.
heart rate or diastolic blood pressure. However, significant differences It should be noted that the presentation of affective pictures itself
were found for systolic blood pressure (F(2,150) = 5.47, p = .011, elicits a cardiovascular response and thus may have influenced the
η² = .068; main effect “affective context”). Analysis of contrasts cardiovascular response to startle stimuli. In accordance, we observed
indicated a significant increase of systolic blood pressure in pleasant a significant increase of systolic (but not diastolic) blood pressure in
compared to neutral or unpleasant context (p = 0.021). Regression response to the presentation of pleasant (compared to neutral)
analyses were performed in a similar way as for the response to startle pictures without startle stimulus presentation. This increase of
stimuli. Anger out was negatively correlated with the systolic (ß = systolic blood pressure may reflect an activation of the sympathetic
−.277, t = − 2.481, p = .015) and diastolic (ß = −.234, t = − 2.074, nervous system that would be in line with the increased response to
p = .042) blood pressure response to unpleasant pictures. Further- the subsequent startle stimulus presentation. Increased baseline
more, age was negatively correlated with diastolic blood pressure
responses to neutral pictures (ß = −.230, t = − 2.034, p = .045), and
physical activity was positively correlated with systolic blood
pressure responses to pleasant pictures (ß = .250, t = 2.220, p = .029).
Collinearity diagnostics were performed on all regression models.
Only the systolic blood pressure in unpleasant context showed a
Condition Index above 30, indicating a moderate degree of collinearity
(CI: 34.98). However, variance–decomposition proportions associated
with the high Condition Index were less than 0.50 for all included
variables, thus none of the variables was excluded from the model.

4. Discussion

Startle stimuli elicited significant heart rate and blood pressure


responses that were modulated by affective context. Trait-anger
differentially influenced the cardiovascular reaction to startle stimuli
depending on affective context. We could replicate a significant
cardiovascular response to startle stimuli. To our knowledge, there
have only been three previous publications reporting a blood pressure
response to startle stimuli (Girard et al., 2001; Holand et al., 1999a;
Holand et al., 1999b). However, this is the first study that investigated
the influence of affective context on the blood pressure response. In Fig. 5. Correlation of maximum diastolic blood pressure responses to startle stimuli
contrast to the expected pattern of modulation (along the valence during unpleasant context and anger-in (mean of all participants, n = 76).
S. Richter et al. / International Journal of Psychophysiology 79 (2011) 364–370 369

blood pressure in turn activates the baroreflex and may therefore alter (i.e. passive listening to loud noises as employed in the present task)
the heart rate response to startle stimuli in pleasant context. This may be more related to a passive coping task. Therefore, task design
finding may help to explain the inconsistent results for heart rate may have contributed to the observed association of anger-out with
responses in pleasant context reported in previous studies (Bradley lower (instead of higher) blood pressure responses, as well as the fact
and Lang, 2000; Sanchez et al., 2002). The increased systolic blood that anger-in (a trait more related to passive coping) emerged as a
pressure in response to pleasant pictures may also have obscured better predictor for blood pressure reactivity in the present study.
effects of anger-in on the blood pressure response in pleasant context. The association of family history of hypertension with blood
In contrast, the blood pressure response did not differ between pressure reactivity and subjective ratings of pleasant stimulus
unpleasant and neutral pictures, although unpleasant pictures were material suggest a more general, hereditary (or acquired) difference
rated as even more arousing than pleasant pictures. A possible in autonomic nervous system responsiveness and affective stimulus
explanation may be that the cardiovascular response to affective processing. Furthermore, trait anger was associated with higher
stimuli differs significantly for different subcategories of unpleasant (anger-in) and lower (anger-out) blood pressure responses in neutral
valence, such as anger, fear or disgust etc. (Christie and Friedman, context, and anger-out was associated with a more positive
2004; Lerner et al., 2007). Importantly, EMG responses did not evaluation of pleasant pictures. These findings support the assump-
correlate with trait anger, suggesting similar reflex magnitudes. tion of a general bias in affective stimulus processing associated with
Arousal ratings for unpleasant pictures correlated positively with trait anger. The trait anger-out may be associated with a bias towards
anger-in score of the STAXI questionnaire that was also the most positive stimulus perception, while anger-in may be associated with a
important determinant of blood pressure responsiveness in unpleas- bias towards negative stimulus perception. As previously hypothe-
ant context. These results underline the importance of a psychological sized, such differences in perception may cause greater arousal in
trait (anger-in) for sympathetic reactivity as reflected by blood subjects with high anger-in (Jorgensen et al., 1996), resulting in
pressure reactivity, especially in situations that induce negative enhanced cardiovascular reactivity (Bongard et al., 1998; Vogele et al.,
emotions. In contrast heart rate responses, governed by vagal activity 1997), especially in unpleasant context, promoting the development
(de Marneffe et al., 1993) were not affected, suggesting that of later hypertensive disease (Schlaich et al., 2004). Thus, our results
parasympathetic control of the heart is not influenced by trait back Alexander who earlier postulated such a role of anger in the
anger. These results support an association of trait anger and etiology of hypertension (Alexander, 1939).
increased sympathetic activity in the etiology of hypertensive disease. Some limitations need to be considered. This study was not
They furthermore suggest that (subjective) arousal, rather than designed to investigate the underlying mechanisms of autonomic
emotion, constitutes the link between the psychological trait and activation. We could demonstrate an impact of trait anger on
autonomic nervous system reactivity. However, it may be that cardiovascular responses to startle stimuli in different affective
participants with higher scores of “anger-in” suppress their negative context, but the mechanisms remain to be clarified in future research.
emotions to a higher degree, resulting in similar valence ratings in The modulation of the blood pressure responses to startle stimuli by
spite of stronger emotional reactions to foreground stimulation. arousal was not expected because similar patterns of modulation have
Heart rate responsiveness and blood pressure responsiveness in previously not been described in the literature. To further elucidate
neutral context were negatively correlated with physical activity, the role of arousal in the modulation of the blood pressure responses
probably reflecting an increased parasympathetic tone (Sharma and to startle stimuli, a study including systematic variation of the arousal
Deepak, 2004; Sztajzel et al., 2006) or increased baroreflex control of inherent in the presented stimuli would be needed. We examined
the heart rate (Raczak et al., 2005; Ueno and Moritani, 2003) that are young healthy Caucasian males. Therefore, results cannot be gener-
believed to mediate the beneficial effects of physical activity on the alized to older people, females, participants with different ethnic
cardiovascular system (Sharma and Deepak, 2004). Indeed, a recent background or patients with cardiovascular diseases. Even though it
study found enhanced baroreflex sensitivity that was mainly was our explicit goal to investigate the effect of anger in healthy
associated with vagal activation in physically active students participants, a further investigation of these potential influencing
(Martin-Vazquez and Reyes Del Paso, 2010). factors might be useful.
Our results match previous studies that consistently observed an In conclusion, we could demonstrate that blood pressure
association of anger-in with higher blood pressure reactivity (Burns, responses, in contrast to heart rate responses, were modulated by
1995; Holroyd and Gorkin, 1983; Mills and Dimsdale, 1993; Vogele the arousal inherent in the foreground stimulation. These findings
and Steptoe, 1992). We could extend these findings by demonstrating suggest sympathetic activation with higher arousal (independent of
the importance of affective context for this relationship. The observed valence) and parasympathetic (co-)activation in pleasant, but not in
association of anger-out with lower cardiovascular responses to unpleasant, context. Higher scores for anger-in were associated with
startle stimuli (as well as blood pressure responses to unpleasant enhanced subjective arousal and enhanced blood pressure respon-
pictures) is in line with previous reports investigating cardiovascular siveness, especially in unpleasant context, suggesting higher sympa-
reactivity during stressful tasks (Holroyd and Gorkin, 1983; Vogele thetic reactivity as a consequence of affective context. A positive
and Steptoe, 1992). However, opposite results have also been correlation of family history of hypertension and blood pressure
reported (Burns, 1995; Faber and Burns, 1996; Haeri et al., 1996; responsiveness in unpleasant context may suggest a hereditary
Vogele and Steptoe, 1992). This inconsistency may be due to component. Our results support the hypothesized association be-
differences in task design (Garcia-Leon et al., 2003; Vogele and tween the psychological trait anger-in (that is associated with the
Steptoe, 1992). Positive correlations of trait anger and blood pressure suppressed anger construct) in unpleasant context and enhanced
reactivity were most consistently reported for active coping tasks cardiovascular reactivity. Long-term follow up studies have to show if
(Burns, 1995; Faber and Burns, 1996; Haeri et al., 1996). In line with this pattern of enhanced sympathetic reactivity in unpleasant context
this, Vogele and Steptoe found a positive correlation of anger-out and is a risk factor for the development of essential hypertension.
systolic blood pressure reactivity during a mirror drawing task, but a
negative correlation during a non-verbal arithmetic task within the
same study population. Acknowledgement
The startle reflex is brainstem relayed and responses are elicited
before a conscious evaluation of the stimulus is possible. However, the The study was part of an ongoing project on salt sensitivity and
continuing cardiovascular response may be modulated by higher stress reactivity of Hans-Christian Deter supported by the Deutsche
cognitive processes after the response onset, and the general setting Forschungsgemeinschaft (DE224/6-1).
370 S. Richter et al. / International Journal of Psychophysiology 79 (2011) 364–370

References Lang, P.J., Bradley, M.M., Cuthbert, B.N., 1990. Emotion, attention, and the startle reflex.
Psychol Rev 97, 377–395.
Alexander, F.G., 1939. Emotional factors in essential hypertension. Psychosom Med 1, Lawler, K.A., Kline, K., Seabrook, E., Krishnamoorthy, J., Anderson, S.F., Wilcox, Z.C.,
175–179. Craig, F., Adlin, R., Thomas, S., 1998. Family history of hypertension: a
Bongard, S., al'Absi, M., 2005. Domain-specific anger expression and blood pressure in psychophysiological analysis. Int J Psychophysiol 28, 207–222.
an occupational setting. J Psychosom Res 58, 43–49. Lerner, J.S., Dahl, R.E., Hariri, A.R., Taylor, S.E., 2007. Facial expressions of emotion reveal
Bongard, S., al'Absi, M., Lovallo, W.R., 1998. Interactive effects of trait hostility and anger neuroendocrine and cardiovascular stress responses. Biol Psychiatry 61, 253–260.
expression on cardiovascular reactivity in young men. Int J Psychophysiol 28, Mancia, G., Grassi, G., Giannattasio, C., Seravalle, G., 1999. Sympathetic activation in the
181–191. pathogenesis of hypertension and progression of organ damage. Hypertension 34,
Bradley, M.M., Lang, P.J., 1994. Measuring emotion: the Self-Assessment Manikin and 724–728.
the Semantic Differential. J Behav Ther Exp Psychiatry 25, 49–59. Markovitz, J.H., Matthews, K.A., Kannel, W.B., Cobb, J.L., D'Agostino, R.B., 1993.
Bradley, M.M., Lang, P.J., 2000. Affective reactions to acoustic stimuli. Psychophysiology Psychological predictors of hypertension in the Framingham Study. Is there
37, 204–215. tension in hypertension? Jama 270, 2439–2443.
Bradley, M.M., Cuthbert, B.N., Lang, P.J., 1990. Startle reflex modification: emotion or Martin-Vazquez, M., Reyes Del Paso, G.A., 2010. Physical training and the dynamics of
attention? Psychophysiology 27, 513–522. the cardiac baroreflex: a comparison when blood pressure rises and falls. Int J
Buchholz, K., Schachinger, H., Wagner, M., Schorr, U., Sharma, A.M., Deter, H.C., 2001. Psychophysiol 76, 142–147.
Enhanced affective startle modulation in salt-sensitive subjects. Hypertension 38, McCraty, R., Atkinson, M., Tiller, W.A., Rein, G., Watkins, A.D., 1995. The effects of
1325–1329. emotions on short-term power spectrum analysis of heart rate variability. Am J
Burns, J.W., 1995. Interactive effects of traits, states, and gender on cardiovascular Cardiol 76, 1089–1093.
reactivity during different situations. J Behav Med 18, 279–303. Miller, M.W., Patrick, C.J., Levenston, G.K., 2002. Affective imagery and the startle
Christie, I.C., Friedman, B.H., 2004. Autonomic specificity of discrete emotion and response: probing mechanisms of modulation during pleasant scenes, personal
dimensions of affective space: a multivariate approach. Int J Psychophysiol 51, experiences, and discrete negative emotions. Psychophysiology 39, 519–529.
143–153. Mills, P.J., Dimsdale, J.E., 1993. Anger suppression: its relationship to beta-adrenergic
Cook III, E.W., Davis, T.L., Hawk, L.W., Spence, E.L., Gautier, C.H., 1992. Fearfulness and receptor sensitivity and stress-induced changes in blood pressure. Psychol Med 23,
startle potentiation during aversive visual stimuli. Psychophysiology 29, 633–645. 673–678.
de Marneffe, M., Gregoire, J.M., Waterschoot, P., Kestemont, M.P., 1993. The sinus node Raczak, G., Pinna, G.D., La Rovere, M.T., Maestri, R., Danilowicz-Szymanowicz, L.,
function: normal and pathological. Eur Heart J 14, 649–654. Ratkowski, W., Figura-Chmielewska, M., Szwoch, M., Ambroch-Dorniak, K., 2005.
Deter, H.C., Buchholz, K., Schorr, U., Mathiak, K., Sharma, A.M., 2001. Salt-sensitivity and Cardiovagal response to acute mild exercise in young healthy subjects. Circ J 69,
other predictors of stress-related cardiovascular reactivity in healthy young males. 976–980.
Clin Exp Hypertens 23, 213–225. Sanchez, M., Ruiz-Padial, E., Perez, N., Fernandez, P., Cobos, P., Vila, J., 2002. Modulacion
Dimsdale, J.E., Pierce, C., Schoenfeld, D., Brown, A., Zusman, R., Graham, R., 1986. emocional de los reflejos defensivos mediante visualizacion de imagenes afectivas.
Suppressed anger and blood pressure: the effects of race, sex, social class, obesity, Psicotema 14, 702–707.
and age. Psychosom Med 48, 430–436. Sanchez-Navarro, J.P., Martinez-Selva, J.M., Torrente, G., Roman, F., 2008. Psychophysio-
Durel, L.A., Carver, C.S., Spitzer, S.B., Llabre, M.M., Weintraub, J.K., Saab, P.G., logical, behavioral, and cognitive indices of the emotional response: a factor-analytic
Schneiderman, N., 1989. Associations of blood pressure with self-report measures study. Span J Psychol 11, 16–25.
of anger and hostility among black and white men and women. Health Psychol 8, Schlaich, M.P., Lambert, E., Kaye, D.M., Krozowski, Z., Campbell, D.J., Lambert, G.,
557–575. Hastings, J., Aggarwal, A., Esler, M.D., 2004. Sympathetic augmentation in
Ewart, C.K., Kolodner, K.B., 1994. Negative affect, gender, and expressive style predict hypertension: role of nerve firing, norepinephrine reuptake, and angiotensin
elevated ambulatory blood pressure in adolescents. J Pers Soc Psychol 66, 596–605. neuromodulation. Hypertension 43, 169–175.
Faber, S.D., Burns, J.W., 1996. Anger management style, degree of expressed anger, and Schum, J.L., Jorgensen, R.S., Verhaeghen, P., Sauro, M., Thibodeau, R., 2003. Trait anger,
gender influence cardiovascular recovery from interpersonal harassment. J Behav anger expression, and ambulatory blood pressure: a meta-analytic review. J Behav
Med 19, 31–53. Med 26, 395–415.
Ferriss, J.B., 1978. The pathogenesis of essential hypertension. Invest Cell Pathol 1, Schwenkmezger, P., Hodapp, V., 1991. A questionnaire for assessing anger and
171–197. expression of anger. Z Klin Psychol Psychopathol Psychother 39, 63–68.
Forgays, D.G., Forgays, D.K., Spielberger, C.D., 1997. Factor structure of the State-Trait Shapiro, D., Goldstein, I.B., Jamner, L.D., 1995. Effects of anger/hostility, defensiveness,
Anger Expression Inventory. J Pers Assess 69, 497–507. gender, and family history of hypertension on cardiovascular reactivity. Psycho-
Garcia-Leon, A., Reyes del Paso, G.A., Robles, H., Vila, J., 2003. Relative effects of physiology 32, 425–435.
harassment, frustration, and task characteristics on cardiovascular reactivity. Int J Shapiro, D., Jamner, L.D., Goldstein, I.B., 1997. Daily mood states and ambulatory blood
Psychophysiol 47, 159–173. pressure. Psychophysiology 34, 399–405.
Gautier, C.H., Cook III, E.W., 1997. Relationships between startle and cardiovascular Sharma, R.K., Deepak, K.K., 2004. A short duration of physical training benefits
reactivity. Psychophysiology 34, 87–96. cardiovascular performance. Indian J Physiol Pharmacol 48, 481–485.
Girard, A., Holand, S., Laude, D., Elghozi, J.L., 2001. Antihypertensive monotherapy and Spicer, J., Chamberlain, K., 1996. Cynical hostility, anger, and resting blood pressure. J
cardiovascular responses to an acoustic startle stimulus. J Cardiovasc Pharmacol 37, Psychosom Res 40, 359–368.
101–107. Spielberger, C.D., 1988. State-Trait-Anger-Expression-Inventory (STAXI). Research
Haeri, S.L., Mills, P.J., Nelesen, R.A., Berry, C.C., Ziegler, M.G., Dillon, E., Dimsdale, J.E., Edition ed, Psychological Assessment Ressources, Odessa, Florida, USA.
1996. Acute psychologic stress reactivity in blacks versus whites:relationship to Sztajzel, J., Atchou, G., Adamec, R., Bayes de Luna, A., 2006. Effects of extreme endurance
psychologic characteristics. Blood Press Monit 1, 27–32. running on cardiac autonomic nervous modulation in healthy trained subjects. Am
Holand, S., Girard, A., Laude, D., Meyer-Bisch, C., Elghozi, J.L., 1999a. Effects of an J Cardiol 97, 276–278.
auditory startle stimulus on blood pressure and heart rate in humans. J Hypertens Ueno, L.M., Moritani, T., 2003. Effects of long-term exercise training on cardiac
17, 1893–1897. autonomic nervous activities and baroreflex sensitivity. Eur J Appl Physiol 89,
Holand, S., Girard, A., Meyer-Bisch, C., Elghozi, J.L., 1999b. Cardiovascular responses to a 109–114.
acoustic startle stimulus in man. Arch Mal Coeur Vaiss 92, 1127–1131. Vanman, E.J., Boehmelt, A.H., Dawson, M.E., Schell, A.M., 1996. The varying time courses of
Holroyd, K.A., Gorkin, L., 1983. Young adults at risk for hypertension: effects of family attentional and affective modulation of the startle eyeblink reflex. Psychophysiology
history and anger management in determining responses to interpersonal conflict. 33, 691–697.
J Psychosom Res 27, 131–138. Vogele, C., Steptoe, A., 1992. Emotional coping and tonic blood pressure as
Igna, C.V., Julkunen, J., Vanhanen, H., 2009. Anger expression styles and blood pressure: determinants of cardiovascular responses to mental stress. J Hypertens 10,
evidence for different pathways. J Hypertens 27, 1972–1979. 1079–1087.
Jorgensen, R.S., Johnson, B.T., Kolodziej, M.E., Schreer, G.E., 1996. Elevated blood Vogele, C., Jarvis, A., Cheeseman, K., 1997. Anger suppression, reactivity, and
pressure and personality: a meta-analytic review. Psychol Bull 120, 293–320. hypertension risk: gender makes a difference. Ann Behav Med 19, 61–69.
Lang, P.J., Öhman, A., Vaitl, D., 1988. The International Affective Picture System
(photographic slides). University of Florida, Gainsville, Florida, USA.

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