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Gender-specific effects of trait anxiety on the cardiac defense response
Personality and Individual Differences 96 (2016) 243–247
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Gender-specific effects of trait anxiety on the cardiac defense response Raúl López ⁎,1, Rosario Poy, Pilar Segarra, Àngels Esteller, Alicia Fonfría, Pablo Ribes, Carlos Ventura, Javier Moltó ⁎ Affective Neuroscience Lab, Department of Basic and Clinical Psychology, and Psychobiology, Universitat Jaume I, Avenida Sos Baynat, s/n, 12071 Castellón, Spain
a r t i c l e
i n f o
Article history: Received 14 September 2015 Received in revised form 20 January 2016 Accepted 7 March 2016 Available online xxxx Keywords: Anxiety Gender Cardiac defense response
a b s t r a c t This study examined the association between trait anxiety and the reactivity of the defensive motivational system, as indexed by the cardiac defense response (CDR) to an unexpected, intense noise, in a mixed-gender undergraduate sample. Gender-specific effects were observed: only women showed an association between trait anxiety and the CDR, consisting of a more intense, prompter, and durable defensive response in high-anxious women. This association was not evident during the first component of the defensive response — identified as an attentional process of stimulus rejection — but in later components reflecting attentional orienting and motivational processes of energetic mobilization for setting an active defensive response — which might suggest reduced parasympathetic dominance along with increased sympathetic dominance. These findings in an unselected sample are consistent with the proposal of a more reactive defensive motivational system as a potential vulnerability factor towards anxiety manifestations in women. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction
various situations. Gender differences in trait anxiety could also be explained by other factors such as women's higher symptom perception (Gijsbers van Wijk & Kolk, 1997) and/or men's inhibition to report symptoms of anxiety (Bekker & van Mens-Verhulst, 2007).
Emotions are organized in two basic motivational systems that evolved from primitive neural circuits in mammals: the appetitive motivational system — associated with approach to food, sexual and caregiving behaviors —, and the defensive motivational system — associated with avoidance, flight and fight protective behaviors, which is regarded as the neural basis of fear and anxiety (Lang, Davis, & Öhman, 2000). From this perspective, anxiety is defined as an emotional state with an adaptive function in situations entailing danger for the survival of the organism. However, if such adaptive defensive state appears in the absence of an actual threat, or its magnitude is disproportionate in relation to the intensity of the danger, anxiety could become pathological. Of particular importance to this study, the probability of suffering pathological anxiety is greater for women than men: women have higher risk of suffering an anxiety disorder than men in adulthood (Bruce et al., 2005), childhood (Anderson, Williams, McGee, & Silva, 1987), and adolescence (Bowen, Offord, & Boyle, 1990; McGee et al., 1990). Consistent with these gender differences, women show higher levels of trait anxiety (de Visser et al., 2010; McCleary & Zucker, 1991), suggesting a greater proneness to react with elevate anxiety to
Physiological response has been central in the scientific study of anxiety since it constitutes an objective and quantifiable measure of cognitive and emotional processes involved in anxiety disorders (cf. Barlow & Wolfe, 1981) and, more specifically, measures of autonomic nervous system (ANS) activation have been the predominant psychophysiological tool in anxiety research (cf. Edgar, Keller, Heller, & Miller, 2007). Thus, at a physiological level, human anxiety states produced by a specific prompt are consistently characterized by a pattern of reciprocal activation of the sympathetic (SNS) branch of the ANS and parasympathetic (PNS) deactivation, along with faster and shallower respiration: specifically, sympathetic activation results in physiological changes such as skin conductance, blood pressure, and heart rate increase, while parasympathetic inhibition is reflected in decreased heart rate variability (see Kreibig, 2010, for a review).2
⁎ Corresponding authors. E-mail addresses: [email protected] (R. López), [email protected] (R. Poy), [email protected] (P. Segarra), [email protected] (À. Esteller), [email protected] (A. Fonfría), [email protected] (P. Ribes), [email protected] (C. Ventura), [email protected] (J. Moltó). 1 Present address: Department of Applied Pedagogy and Educational Psychology, Universitat de les Illes Balears, Ctra. de Valldemossa, km 7.5, 07122 Palma de Mallorca, Illes Balears, Spain.
2 Anxiety has also found to be associated with somatic reflex (e.g., startle) potentiation (see Grillon, 2008), though results remain somewhat inconsistent. Enhanced startle potentiation has been related to negative emotional traits (fearfulness, behavioral inhibition, harm avoidance) that predispose individuals to anxiety disorders but, in contrast, other studies found no relationship between startle modulation and characteristics of anxiety, including anxious apprehension, negative affectivity and trait anxiety (see Vaidyanathan, Patrick, & Cuthbert, 2009, for a review).
http://dx.doi.org/10.1016/j.paid.2016.03.014 0191-8869/© 2016 Elsevier Ltd. All rights reserved.
1.1. The physiology of anxiety
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The use of psychophysiological measures of ANS activation for exploring vulnerability towards the development of anxiety disorders has revealed the existence of distinct gender-specific relations, in line with clinical data (see Kessler et al., 1994). For example, social phobia and state anxiety have been associated with autonomic hyperreactivity in response to stress produced by a public speech in women, but not in men (Carrillo et al., 2001; Grossman, Wilhelm, Kawachi, & Sparrow, 2001). In this line, social phobia has also been related to reductions in autonomic cardiac control — as indexed by diminished HRV — in female, but not in male, patients (Alvares et al., 2013). 1.2. Cardiac defense response as an index of defensive reactivity and anxiety Change in heart rate (HR) is considered one of the most reliable measures for studying heightened psychophysiological reactivity, being widely used as a marker of defensive reactivity in anxiety disorders (see Pole, 2007). However, as HR is regulated by both the SNS and the PNS, the above-mentioned HR increases associated with anxiety states could be due to SNS activation, PNS withdrawal, or both (cf. Bernston, Cacioppo, & Quigley, 1993). In contrast to simple measures of overall change in HR, the cardiac defense response (CDR) — a phasic HR response with alternating accelerative and decelerative components distinctively linked to parasympathetic and sympathetic mediating mechanisms (cf. Fernández & Vila, 1989; Reyes del Paso, Godoy, & Vila, 1993) — could provide a more detailed characterization of the sympathetic–parasympathetic mediation of cardiac changes in anxiety, as well as of psychological processes involved, since it allows to track the transition from attentional to emotional processes that sequentially occur in the defensive response. The CDR is a dynamic pattern of cardiac reactivity in response to aversive, discrete, intense, and unexpected stimulation, usually acoustic (Fernández & Vila, 1989). The CDR consists of two successive accelerations and decelerations in HR. The first accelerative/decelerative component is mediated by the inhibition/activation of the parasympathetic branch of the ANS (Reyes del Paso et al., 1993). The first acceleration peaks at around 3–4 s after stimulus onset — being interpreted as part of an attentional process of stimuli rejection that interrupts the ongoing activity of the organism (Vila et al., 2007) —, and then HR drops to baseline level or even lower. This decrement in HR has been interpreted as an orienting attentional response focused on searching the aversive stimulus in the environment (Fernández & Vila, 1989). Following the first deceleration, a second accelerative/decelerative component, mainly mediated by the sympathetic branch of the ANS, appears. This late accelerative component, which maximum acceleration is usually observed 20 to 45 s after stimulus onset, has been interpreted as a motivational process involved in mobilization of energetic resources to set a defensive coping response (Fernández & Vila, 1989). The final component of the CDR is a recovery phase, lasting until 80 s after stimulus onset, in which HR returns to basal levels in the case of no actual danger occurs (Vila et al., 2007). This dynamic sequence of the cardiac reactivity pattern is congruent with the defense cascade model (see Lang, Bradley, & Cuthbert, 1997) describing the time course of defensive reactions, from attention to action preparation: defensive reactions begin with predominantly attentional orienting responses that focus on detecting and analyzing potentially dangerous stimuli, and then change to late motivational/emotional responses linked to active defense such as escape or aggression.3 Consistent with this model, the second 3 Although the fight-or-flight characterization of the human stress response does not accurately describe the behavioral response of women, who seem to show an oxytocin mediated tend-and-befriend response to stress — with tending responses including nurturing activities designed to protect the self and offspring, promote safety, and reduce distress, and befriending behaviors creating and maintaining social networks —, the primary autonomic and neuroendocrine core of stress responses does not vary substantially between men and women, with both genders showing sympathetic activation in response to the perception of threat (see Taylor et al., 2000, for a thorough review).
accelerative component of the CDR has found to be a valid index of the activation of the defensive motivational system (see, for example, Ramírez, Sánchez, Fernández, Lipp, & Vila, 2005), as well as a reliable predictor of the acquisition and maintenance of fear learning (López, Poy, Pastor, Segarra, & Moltó, 2009). Interestingly, some evidence exists in women for an advanced and intensified motivational phase of the CDR — i.e., its second accelerative component — as a function of excessive worry (Delgado et al., 2009) and the presence of post-traumatic stress disorder diagnosis (Schalinski, Elbert, & Schauer, 2013). Based on the assumption that this characteristic pattern of enhanced defensive cardiac reactivity could become a useful index of vulnerability towards anxiety disorders, this study was aimed to experimentally explore, for the first time in literature, the role of gender in the association between trait anxiety and the reactivity of the defensive motivational system as indexed by the CDR in a non-clinical sample. In view of previous studies on this topic (Delgado et al., 2009; Schalinski et al., 2013), we expected that trait anxiety would be positively associated with enhanced defensive reactivity as indexed by the second accelerative component of the CDR. Additionally, based on evidence showing gender differences in the prevalence of anxiety disorders (Kessler et al., 1994) and gender-specific effects on autonomic markers of anxiety (Alvares et al., 2013; Carrillo et al., 2001; Grossman et al., 2001), we also examined whether gender might affect this expected association. To this end, we measured the CDR in healthy men and women assessed for trait anxiety using the Trait Anxiety scale of the State–Trait Anxiety Inventory (STAI-T; Spielberger, Gorsuch, & Lushene, 1970). 2. Method 2.1. Participants and procedure Participants were 75 undergraduates (33 men) from the Universitat Jaume I of Castellón (Spain) aged between 17 and 27 (M = 19.61, SD = 2.07), involved in a wider investigation about personality and emotional reactivity. None were undergoing psychiatric or pharmacological treatment, and none presented visual, auditory or cardiovascular deficits. All participants provided informed consent, completed the STAI-T in group sessions of 20–50 students and, between one to two weeks later, participated individually in a psychophysiological reactivity test to obtain the CDR. 2.2. Materials and design The Trait Anxiety scale (STAI-T) of the State–Trait Anxiety Inventory (Spielberger et al., 1970) contains 20 statements concerning cognitive and somatic components of anxiety as a general personality trait; each item is answered on a 4-point Likert scale — from “almost never” to “almost always”. In the current study, α coefficient was .89. 2.2.1. Defense psychophysiological test The test to obtain the CDR (cf. Vila et al., 2007) consisted of a rest period of 8 min (with no stimulation) followed by the unexpected presentation of an intense auditory stimulus — 500 ms, 105 dB, instantaneous risetime white noise —, delivered binaurally throughout 3a Insert Earphone (Eartone). Electrocardiogram recording lasted from 15 s prior to stimulus onset (baseline) to 80 s after its presentation. Each participant completed the task individually sat in a comfortable armchair in an isolated, semi-darkened room. 2.3. Data recording, reduction, and statistical analyses Stimuli control and electrocardiogram acquisition were accomplished using VPM software (Cook, 2002). Ag/AgCl surface electrodes (Standard Lead II) filled with hypertonic electrolyte paste provided 1000 samples/second electro-cardiograph analogical
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signals to a Coulbourn V75-04 High Gain Bioamplifier, and then to a Coulbourn V77-26 Tachometer. White noise was produced by a Coulbourn S81-02 generator and gated through a Coulbourn S82-24 audio-mixer amplifier. After recording, Matlab software KARDIA v.2.7 (Perakakis, Joffily, Taylor, Guerra, & Vila, 2010) was used for detecting and correcting artifacts in the electrocardiogram and for reducing data in order to obtain the CDR for each participant. Data for the 80-s recording period were transformed to averages for every second, and HR change scores were computed by subtracting the pretrial 15-s baseline average. To facilitate statistical analysis, the 80 second-by-second HR change scores were reduced to ten values corresponding to the medians of 10 progressively longer intervals (cf. Vila et al., 2007): seconds 1–3, 4–6, 7–11, 12–16, 17–23, 24–30, 31–37, 38–50, 51–63 and 64–76 (from this point on, M1 to M10). This procedure results in a simplified representation of the CDR without altering its characteristic pattern, with M1 reflecting the first acceleration, M2 to M4 reflecting the first deceleration, M5 to M8 reflecting the second acceleration, and M9 to M10 reflecting the second deceleration (Vila et al., 2007). Heart rate data was examined by conducting a 2 (Gender) × 10 (Median) repeated measures general linear model (GLM) in which scores on STAI-T were included as a continuous between-subjects factor. Greenhouse–Geisser correction was applied to effects involving repeated measures (Jennings, 1987; Vasey & Thayer, 1987). Significant effects of gender on the anxiety–CDR association were examined by performing separate 10 (Median) repeated measures GLMs, including scores on STAI-T as a continuous between-subjects factor, for men and women. In addition, to further examine associations between anxiety and the time course of the CDR, continuous scores on STAI-T were entered in simple regression analyses predicting each CDR median for men and women separately.
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main effects of Gender, F(1, 74) = 9.21, p b .005, η2p = .12, and STAI-T, F(1, 74) = 6.16, p b .02, η2p = .08, as well as a significant Gender × STAI-T interaction, F (1, 74) = 12.95, p b .0005, η2p = .15, suggesting that the effect of trait anxiety on the CDR average across medians varied as a function of gender. Gender effects on the anxiety–CDR association were then pursued by conducting analyses for men and women separately. For women, the GLM revealed a significant main effect of STAI-T scores on HR change scores, F(1, 41) = 13.96, p b .0005, η2p = .26, with higher levels of trait anxiety associated with larger CDR averages across medians, β = .51, t(40) = 3.74, p b .001. Subsequent simple regression analyses revealed that STAI-T scores accounted for a significant proportion of variance in greater cardiac reactivity during the first deceleration (except for M2) and the second accelerative/decelerative component, but not during the first acceleration of the CDR (that is, for M1; see Table 2). For men, neither the GLM nor the regression analyses revealed any significant effects of STAI-T scores on HR change scores (all Fs b 1 and all ps N .09, respectively). In order to make results more illustrative, women were assigned to High (n = 22) or Low (n = 20) Anxiety groups according to whether their STAI-T score was above or below the median of the experimental sample (Mdn = 24.00). As expected, participants in the High Anxiety group scored higher than participants in the Low Anxiety group in STAI-T (M = 30.50, SD = 6.79 for the High, and M = 16.75, SD = 5.13 for the Low Anxiety group, respectively), t(40) = 7.35, p b .001. Consistent with the simple regression results for women, independent samples t-tests for each median revealed that high-anxious women showed significantly greater HR changes than low-anxious women from M3 to M10, ts(40) N 2.22, ps b .05, but not in earlier medians (M1 and M2, ps N .19; see Fig. 1). 4. Discussion
3. Results 3.1. Trait anxiety in men and women There were no significant differences between men and women in STAI-T (20.72 vs. 23.95, respectively; p = .17). 3.2. Trait anxiety and cardiac defense response in men and women The GLM in the sample as a whole showed a significant main effect of Median, F(9, 66) = 9.37, p b .0001, η2p = .12, that confirmed the presence of a typical CDR pattern with a first accelerative component peaking at M1, an early decelerative component lasting to M4, a second accelerative component consisting of M5, M6 and M7, and then a late deceleration extending to M10 (see Table 1). Women showed higher HR change scores than men only for M2, t(73) = 3.10, p b .005 (remaining medians ps N .11), Gender × Median interaction F(9, 66) = 2.76, p b .05, η2p = .04. Analyses also revealed significant Table 1 Mean (standard deviation) for CDR medians in the overall sample (N = 75) and for men (n = 33) and women (n = 42). Median M1 M2 M3 M4 M5 M6 M7 M8 M9 M10
Overall 12.32 5.28 −0.22 −1.66 1.86 4.51 5.55 1.96 −1.64 −2.78
(6.59) (10.54) (10.51) (9.32) (8.22) (8.93) (9.22) (8.21) (6.63) (5.90)
Men 10.96 1.25 −2.03 −2.08 2.23 5.06 5.76 1.85 −1.73 −3.28
Women (6.54) (7.25) (7.60) (7.74) (6.01) (7.44) (7.30) (6.76) (5.74) (5.09)
13.40 8.45 1.20 −1.34 1.57 4.09 5.38 2.05 −1.58 −2.38
(6.50) (11.67) (12.24) (10.49) (9.67) (10.01) (10.57) (9.28) (7.31) (6.50)
Note. Significant differences across gender (Bonferroni's correction for multiple comparisons, p b .005), tested via t-tests for independent samples, are in bold.
The present study examined, in a sample of healthy men and women, the association between trait anxiety, as operationalized by the State–Trait Anxiety Inventory (STAI-T), and the reactivity of the defensive motivational system, as indexed by the cardiac defense response (CDR). Results showed an important moderator effect of gender on the associative pattern of trait anxiety and defensive reactivity: women higher in trait anxiety showed a predominantly accelerative CDR pattern, but anxiety scores were unrelated to the typical CDR pattern found in men. This finding suggests that vulnerability to anxiety disorders involves a gender-specific differential cardiac reactivity to aversive cues, mainly mediated by increased dominance of the sympathetic branch of the autonomic nervous system, and characterized by a more intense, prompter, and durable defensive response for high-anxious women. Specifically, women with higher levels of trait anxiety showed an attenuated early cardiac deceleration and, as hypothesized, a pronounced second accelerative component of the CDR that was also extended in time — consistent with the classic pattern of reciprocal sympathetic
Table 2 Summary of simple regression analyses for CDR medians, using STAI-T scores as predictor, for women (n = 42). Median M1 M2 M3 M4 M5 M6 M7 M8 M9 M10
β
R2
t
p
.16 .25 .33 .45 .44 .52 .45 .43 .40 .45
.03 .06 .11 .20 .19 .27 .20 .18 .16 .21
1.02 1.61 2.22 3.15 3.09 3.84 3.17 2.98 2.74 3.22
.313 .115 .032 .003 .004 b.001 .003 .005 .009 .003
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Fig. 1. Cardiac defense response patterns for women in the High and Low Anxiety groups.
activation and parasympathetic deactivation for anxiety (cf. Kreibig, 2010). Indeed, high-anxious women lacked a true deceleration in the CDR — since HR did not return to baseline levels after the initial acceleration —, suggesting a minimized attentional orienting response towards unexpected, aversive stimuli (i.e., a reduced parasympathetic dominance), and a maximized motivational component of the defensive response (i.e., an increased sympathetic dominance). Additionally, differences associated with trait anxiety lasted throughout the late decelerative component, with a slow return to baseline of cardiac activity in the absence of an actual danger in high-anxious women. Remarkably, high-anxious women showed a first accelerative component commensurate with that of low-anxious women, indicating that this parasympathetic withdrawal-mediated component of the CDR — an index of sensory rejection — does not depend on individual differences in trait anxiety. Conversely, results do suggest a greater predominance of sympathetic vs. parasympathetic activation and a more reactive defensive system in women as a function of increasing dispositional anxiety, consistent with other studies examining the CDR in women with excessive worry (Delgado et al., 2009) or post-traumatic stress disorder (Schalinski et al., 2013). Our results show that, in women alone, anxiety is related to a variation in the temporal course of the defense cascade — that usually begins with an attentional phase followed by a motivational/emotional phase (Lang et al., 1997). It might be possible that the preexisting anxiety state contributes to decrease the threshold for activating the defensive motivational system and to potentiate the coping response to the aversive stimulation, thus diminishing the attentional orienting phase and increasing the motivational components of the defensive reaction in terms of intensity, immediacy and duration (cf. Vila et al., 2007). Beyond, by considering hyperreactivity of the defensive motivational system as a vulnerability factor towards pathological anxiety, our findings seem consistent with prevalence indexes reporting higher proneness to anxiety disorders in women as compared to men (Bruce et al., 2005). Moreover, they add empirical support to the notion of gender-specific associations of clinical anxiety and anxiety vulnerability markers with autonomic hyperreactivity in response to stress (Carrillo et al., 2001; Grossman et al., 2001) and with reductions in autonomic cardiac control as indexed by heart rate variability (Alvares et al., 2013) and, more broadly, to increasing evidence about gender-specific associations in anxiety research across different populations, paradigms, and measures. Thus, gender differences in startle abnormalities have been found in high-risk children (i.e., with a parental history of anxiety disorders) — enhanced fear-potentiated startle in high-risk boys, increased baseline startle in high-risk girls —, suggesting that the vulnerability to anxiety involves a gender-specific differential sensitivity of fear/anxiety pathways (Grillon, Dierker, & Merikangas, 1998). In an event-related brain potentials study about attentional bias in anxiety, anxious women, but not anxious men, displayed greater early visual processing (larger P100 amplitude) to emotional words (Sass et al., 2010). In addition, in a positron emission tomography study, harm avoidance — an anxiety-related personality trait — was negatively correlated with glucose metabolism in the anterior portion of the
ventromedial prefrontal cortex in females but not in males, which suggested gender differences in the association between trait anxiety and autobiographical memory specificity (Hakamata et al., 2009). Selfreported emotion dysregulation plays a greater role in relation to anxiety in girls than it does in boys (Bender, Reinholdt-Dunne, Esbjørn, & Pons, 2012). Finally, high trait anxiety has been directly related to impaired decision-making only in women (de Visser et al., 2010). Overall, these results strongly suggest the existence of a specific phenotypic expression of anxiety in females. At a methodological level, this investigation underscores the utility of the CDR as an indicator of defensive motivational system hyperreactivity in women with a dispositional proneness to react anxiously. Interestingly, our study shows that the effects of high trait anxiety on enhanced cardiovascular response to aversive stimulation can be found at a subclinical level, at least in women. This result is aligned with a dimensional conceptualization of anxiety and supports the appropriateness of studying nonclinical individuals under anxietyprovoking conditions (see Edgar et al., 2007). Notwithstanding this, it would be worthwhile to explore gender-specific endophenotypes of anxiety at clinical levels, using other measures of defensive reactivity (e.g., startle response), in order to clarify the nature and physiological correlates of this broad construct and to help polishing diagnostic and treatment strategies.
Acknowledgments This study was supported by Grant PSI2011-22559 from the Ministerio de Economía y Competitividad (Spain).
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Personality and Individual Differences journal homepage: www.elsevier.com/locate/paid
Gender-specific effects of trait anxiety on the cardiac defense response Raúl López ⁎,1, Rosario Poy, Pilar Segarra, Àngels Esteller, Alicia Fonfría, Pablo Ribes, Carlos Ventura, Javier Moltó ⁎ Affective Neuroscience Lab, Department of Basic and Clinical Psychology, and Psychobiology, Universitat Jaume I, Avenida Sos Baynat, s/n, 12071 Castellón, Spain
a r t i c l e
i n f o
Article history: Received 14 September 2015 Received in revised form 20 January 2016 Accepted 7 March 2016 Available online xxxx Keywords: Anxiety Gender Cardiac defense response
a b s t r a c t This study examined the association between trait anxiety and the reactivity of the defensive motivational system, as indexed by the cardiac defense response (CDR) to an unexpected, intense noise, in a mixed-gender undergraduate sample. Gender-specific effects were observed: only women showed an association between trait anxiety and the CDR, consisting of a more intense, prompter, and durable defensive response in high-anxious women. This association was not evident during the first component of the defensive response — identified as an attentional process of stimulus rejection — but in later components reflecting attentional orienting and motivational processes of energetic mobilization for setting an active defensive response — which might suggest reduced parasympathetic dominance along with increased sympathetic dominance. These findings in an unselected sample are consistent with the proposal of a more reactive defensive motivational system as a potential vulnerability factor towards anxiety manifestations in women. © 2016 Elsevier Ltd. All rights reserved.
1. Introduction
various situations. Gender differences in trait anxiety could also be explained by other factors such as women's higher symptom perception (Gijsbers van Wijk & Kolk, 1997) and/or men's inhibition to report symptoms of anxiety (Bekker & van Mens-Verhulst, 2007).
Emotions are organized in two basic motivational systems that evolved from primitive neural circuits in mammals: the appetitive motivational system — associated with approach to food, sexual and caregiving behaviors —, and the defensive motivational system — associated with avoidance, flight and fight protective behaviors, which is regarded as the neural basis of fear and anxiety (Lang, Davis, & Öhman, 2000). From this perspective, anxiety is defined as an emotional state with an adaptive function in situations entailing danger for the survival of the organism. However, if such adaptive defensive state appears in the absence of an actual threat, or its magnitude is disproportionate in relation to the intensity of the danger, anxiety could become pathological. Of particular importance to this study, the probability of suffering pathological anxiety is greater for women than men: women have higher risk of suffering an anxiety disorder than men in adulthood (Bruce et al., 2005), childhood (Anderson, Williams, McGee, & Silva, 1987), and adolescence (Bowen, Offord, & Boyle, 1990; McGee et al., 1990). Consistent with these gender differences, women show higher levels of trait anxiety (de Visser et al., 2010; McCleary & Zucker, 1991), suggesting a greater proneness to react with elevate anxiety to
Physiological response has been central in the scientific study of anxiety since it constitutes an objective and quantifiable measure of cognitive and emotional processes involved in anxiety disorders (cf. Barlow & Wolfe, 1981) and, more specifically, measures of autonomic nervous system (ANS) activation have been the predominant psychophysiological tool in anxiety research (cf. Edgar, Keller, Heller, & Miller, 2007). Thus, at a physiological level, human anxiety states produced by a specific prompt are consistently characterized by a pattern of reciprocal activation of the sympathetic (SNS) branch of the ANS and parasympathetic (PNS) deactivation, along with faster and shallower respiration: specifically, sympathetic activation results in physiological changes such as skin conductance, blood pressure, and heart rate increase, while parasympathetic inhibition is reflected in decreased heart rate variability (see Kreibig, 2010, for a review).2
⁎ Corresponding authors. E-mail addresses: [email protected] (R. López), [email protected] (R. Poy), [email protected] (P. Segarra), [email protected] (À. Esteller), [email protected] (A. Fonfría), [email protected] (P. Ribes), [email protected] (C. Ventura), [email protected] (J. Moltó). 1 Present address: Department of Applied Pedagogy and Educational Psychology, Universitat de les Illes Balears, Ctra. de Valldemossa, km 7.5, 07122 Palma de Mallorca, Illes Balears, Spain.
2 Anxiety has also found to be associated with somatic reflex (e.g., startle) potentiation (see Grillon, 2008), though results remain somewhat inconsistent. Enhanced startle potentiation has been related to negative emotional traits (fearfulness, behavioral inhibition, harm avoidance) that predispose individuals to anxiety disorders but, in contrast, other studies found no relationship between startle modulation and characteristics of anxiety, including anxious apprehension, negative affectivity and trait anxiety (see Vaidyanathan, Patrick, & Cuthbert, 2009, for a review).
http://dx.doi.org/10.1016/j.paid.2016.03.014 0191-8869/© 2016 Elsevier Ltd. All rights reserved.
1.1. The physiology of anxiety
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The use of psychophysiological measures of ANS activation for exploring vulnerability towards the development of anxiety disorders has revealed the existence of distinct gender-specific relations, in line with clinical data (see Kessler et al., 1994). For example, social phobia and state anxiety have been associated with autonomic hyperreactivity in response to stress produced by a public speech in women, but not in men (Carrillo et al., 2001; Grossman, Wilhelm, Kawachi, & Sparrow, 2001). In this line, social phobia has also been related to reductions in autonomic cardiac control — as indexed by diminished HRV — in female, but not in male, patients (Alvares et al., 2013). 1.2. Cardiac defense response as an index of defensive reactivity and anxiety Change in heart rate (HR) is considered one of the most reliable measures for studying heightened psychophysiological reactivity, being widely used as a marker of defensive reactivity in anxiety disorders (see Pole, 2007). However, as HR is regulated by both the SNS and the PNS, the above-mentioned HR increases associated with anxiety states could be due to SNS activation, PNS withdrawal, or both (cf. Bernston, Cacioppo, & Quigley, 1993). In contrast to simple measures of overall change in HR, the cardiac defense response (CDR) — a phasic HR response with alternating accelerative and decelerative components distinctively linked to parasympathetic and sympathetic mediating mechanisms (cf. Fernández & Vila, 1989; Reyes del Paso, Godoy, & Vila, 1993) — could provide a more detailed characterization of the sympathetic–parasympathetic mediation of cardiac changes in anxiety, as well as of psychological processes involved, since it allows to track the transition from attentional to emotional processes that sequentially occur in the defensive response. The CDR is a dynamic pattern of cardiac reactivity in response to aversive, discrete, intense, and unexpected stimulation, usually acoustic (Fernández & Vila, 1989). The CDR consists of two successive accelerations and decelerations in HR. The first accelerative/decelerative component is mediated by the inhibition/activation of the parasympathetic branch of the ANS (Reyes del Paso et al., 1993). The first acceleration peaks at around 3–4 s after stimulus onset — being interpreted as part of an attentional process of stimuli rejection that interrupts the ongoing activity of the organism (Vila et al., 2007) —, and then HR drops to baseline level or even lower. This decrement in HR has been interpreted as an orienting attentional response focused on searching the aversive stimulus in the environment (Fernández & Vila, 1989). Following the first deceleration, a second accelerative/decelerative component, mainly mediated by the sympathetic branch of the ANS, appears. This late accelerative component, which maximum acceleration is usually observed 20 to 45 s after stimulus onset, has been interpreted as a motivational process involved in mobilization of energetic resources to set a defensive coping response (Fernández & Vila, 1989). The final component of the CDR is a recovery phase, lasting until 80 s after stimulus onset, in which HR returns to basal levels in the case of no actual danger occurs (Vila et al., 2007). This dynamic sequence of the cardiac reactivity pattern is congruent with the defense cascade model (see Lang, Bradley, & Cuthbert, 1997) describing the time course of defensive reactions, from attention to action preparation: defensive reactions begin with predominantly attentional orienting responses that focus on detecting and analyzing potentially dangerous stimuli, and then change to late motivational/emotional responses linked to active defense such as escape or aggression.3 Consistent with this model, the second 3 Although the fight-or-flight characterization of the human stress response does not accurately describe the behavioral response of women, who seem to show an oxytocin mediated tend-and-befriend response to stress — with tending responses including nurturing activities designed to protect the self and offspring, promote safety, and reduce distress, and befriending behaviors creating and maintaining social networks —, the primary autonomic and neuroendocrine core of stress responses does not vary substantially between men and women, with both genders showing sympathetic activation in response to the perception of threat (see Taylor et al., 2000, for a thorough review).
accelerative component of the CDR has found to be a valid index of the activation of the defensive motivational system (see, for example, Ramírez, Sánchez, Fernández, Lipp, & Vila, 2005), as well as a reliable predictor of the acquisition and maintenance of fear learning (López, Poy, Pastor, Segarra, & Moltó, 2009). Interestingly, some evidence exists in women for an advanced and intensified motivational phase of the CDR — i.e., its second accelerative component — as a function of excessive worry (Delgado et al., 2009) and the presence of post-traumatic stress disorder diagnosis (Schalinski, Elbert, & Schauer, 2013). Based on the assumption that this characteristic pattern of enhanced defensive cardiac reactivity could become a useful index of vulnerability towards anxiety disorders, this study was aimed to experimentally explore, for the first time in literature, the role of gender in the association between trait anxiety and the reactivity of the defensive motivational system as indexed by the CDR in a non-clinical sample. In view of previous studies on this topic (Delgado et al., 2009; Schalinski et al., 2013), we expected that trait anxiety would be positively associated with enhanced defensive reactivity as indexed by the second accelerative component of the CDR. Additionally, based on evidence showing gender differences in the prevalence of anxiety disorders (Kessler et al., 1994) and gender-specific effects on autonomic markers of anxiety (Alvares et al., 2013; Carrillo et al., 2001; Grossman et al., 2001), we also examined whether gender might affect this expected association. To this end, we measured the CDR in healthy men and women assessed for trait anxiety using the Trait Anxiety scale of the State–Trait Anxiety Inventory (STAI-T; Spielberger, Gorsuch, & Lushene, 1970). 2. Method 2.1. Participants and procedure Participants were 75 undergraduates (33 men) from the Universitat Jaume I of Castellón (Spain) aged between 17 and 27 (M = 19.61, SD = 2.07), involved in a wider investigation about personality and emotional reactivity. None were undergoing psychiatric or pharmacological treatment, and none presented visual, auditory or cardiovascular deficits. All participants provided informed consent, completed the STAI-T in group sessions of 20–50 students and, between one to two weeks later, participated individually in a psychophysiological reactivity test to obtain the CDR. 2.2. Materials and design The Trait Anxiety scale (STAI-T) of the State–Trait Anxiety Inventory (Spielberger et al., 1970) contains 20 statements concerning cognitive and somatic components of anxiety as a general personality trait; each item is answered on a 4-point Likert scale — from “almost never” to “almost always”. In the current study, α coefficient was .89. 2.2.1. Defense psychophysiological test The test to obtain the CDR (cf. Vila et al., 2007) consisted of a rest period of 8 min (with no stimulation) followed by the unexpected presentation of an intense auditory stimulus — 500 ms, 105 dB, instantaneous risetime white noise —, delivered binaurally throughout 3a Insert Earphone (Eartone). Electrocardiogram recording lasted from 15 s prior to stimulus onset (baseline) to 80 s after its presentation. Each participant completed the task individually sat in a comfortable armchair in an isolated, semi-darkened room. 2.3. Data recording, reduction, and statistical analyses Stimuli control and electrocardiogram acquisition were accomplished using VPM software (Cook, 2002). Ag/AgCl surface electrodes (Standard Lead II) filled with hypertonic electrolyte paste provided 1000 samples/second electro-cardiograph analogical
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signals to a Coulbourn V75-04 High Gain Bioamplifier, and then to a Coulbourn V77-26 Tachometer. White noise was produced by a Coulbourn S81-02 generator and gated through a Coulbourn S82-24 audio-mixer amplifier. After recording, Matlab software KARDIA v.2.7 (Perakakis, Joffily, Taylor, Guerra, & Vila, 2010) was used for detecting and correcting artifacts in the electrocardiogram and for reducing data in order to obtain the CDR for each participant. Data for the 80-s recording period were transformed to averages for every second, and HR change scores were computed by subtracting the pretrial 15-s baseline average. To facilitate statistical analysis, the 80 second-by-second HR change scores were reduced to ten values corresponding to the medians of 10 progressively longer intervals (cf. Vila et al., 2007): seconds 1–3, 4–6, 7–11, 12–16, 17–23, 24–30, 31–37, 38–50, 51–63 and 64–76 (from this point on, M1 to M10). This procedure results in a simplified representation of the CDR without altering its characteristic pattern, with M1 reflecting the first acceleration, M2 to M4 reflecting the first deceleration, M5 to M8 reflecting the second acceleration, and M9 to M10 reflecting the second deceleration (Vila et al., 2007). Heart rate data was examined by conducting a 2 (Gender) × 10 (Median) repeated measures general linear model (GLM) in which scores on STAI-T were included as a continuous between-subjects factor. Greenhouse–Geisser correction was applied to effects involving repeated measures (Jennings, 1987; Vasey & Thayer, 1987). Significant effects of gender on the anxiety–CDR association were examined by performing separate 10 (Median) repeated measures GLMs, including scores on STAI-T as a continuous between-subjects factor, for men and women. In addition, to further examine associations between anxiety and the time course of the CDR, continuous scores on STAI-T were entered in simple regression analyses predicting each CDR median for men and women separately.
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main effects of Gender, F(1, 74) = 9.21, p b .005, η2p = .12, and STAI-T, F(1, 74) = 6.16, p b .02, η2p = .08, as well as a significant Gender × STAI-T interaction, F (1, 74) = 12.95, p b .0005, η2p = .15, suggesting that the effect of trait anxiety on the CDR average across medians varied as a function of gender. Gender effects on the anxiety–CDR association were then pursued by conducting analyses for men and women separately. For women, the GLM revealed a significant main effect of STAI-T scores on HR change scores, F(1, 41) = 13.96, p b .0005, η2p = .26, with higher levels of trait anxiety associated with larger CDR averages across medians, β = .51, t(40) = 3.74, p b .001. Subsequent simple regression analyses revealed that STAI-T scores accounted for a significant proportion of variance in greater cardiac reactivity during the first deceleration (except for M2) and the second accelerative/decelerative component, but not during the first acceleration of the CDR (that is, for M1; see Table 2). For men, neither the GLM nor the regression analyses revealed any significant effects of STAI-T scores on HR change scores (all Fs b 1 and all ps N .09, respectively). In order to make results more illustrative, women were assigned to High (n = 22) or Low (n = 20) Anxiety groups according to whether their STAI-T score was above or below the median of the experimental sample (Mdn = 24.00). As expected, participants in the High Anxiety group scored higher than participants in the Low Anxiety group in STAI-T (M = 30.50, SD = 6.79 for the High, and M = 16.75, SD = 5.13 for the Low Anxiety group, respectively), t(40) = 7.35, p b .001. Consistent with the simple regression results for women, independent samples t-tests for each median revealed that high-anxious women showed significantly greater HR changes than low-anxious women from M3 to M10, ts(40) N 2.22, ps b .05, but not in earlier medians (M1 and M2, ps N .19; see Fig. 1). 4. Discussion
3. Results 3.1. Trait anxiety in men and women There were no significant differences between men and women in STAI-T (20.72 vs. 23.95, respectively; p = .17). 3.2. Trait anxiety and cardiac defense response in men and women The GLM in the sample as a whole showed a significant main effect of Median, F(9, 66) = 9.37, p b .0001, η2p = .12, that confirmed the presence of a typical CDR pattern with a first accelerative component peaking at M1, an early decelerative component lasting to M4, a second accelerative component consisting of M5, M6 and M7, and then a late deceleration extending to M10 (see Table 1). Women showed higher HR change scores than men only for M2, t(73) = 3.10, p b .005 (remaining medians ps N .11), Gender × Median interaction F(9, 66) = 2.76, p b .05, η2p = .04. Analyses also revealed significant Table 1 Mean (standard deviation) for CDR medians in the overall sample (N = 75) and for men (n = 33) and women (n = 42). Median M1 M2 M3 M4 M5 M6 M7 M8 M9 M10
Overall 12.32 5.28 −0.22 −1.66 1.86 4.51 5.55 1.96 −1.64 −2.78
(6.59) (10.54) (10.51) (9.32) (8.22) (8.93) (9.22) (8.21) (6.63) (5.90)
Men 10.96 1.25 −2.03 −2.08 2.23 5.06 5.76 1.85 −1.73 −3.28
Women (6.54) (7.25) (7.60) (7.74) (6.01) (7.44) (7.30) (6.76) (5.74) (5.09)
13.40 8.45 1.20 −1.34 1.57 4.09 5.38 2.05 −1.58 −2.38
(6.50) (11.67) (12.24) (10.49) (9.67) (10.01) (10.57) (9.28) (7.31) (6.50)
Note. Significant differences across gender (Bonferroni's correction for multiple comparisons, p b .005), tested via t-tests for independent samples, are in bold.
The present study examined, in a sample of healthy men and women, the association between trait anxiety, as operationalized by the State–Trait Anxiety Inventory (STAI-T), and the reactivity of the defensive motivational system, as indexed by the cardiac defense response (CDR). Results showed an important moderator effect of gender on the associative pattern of trait anxiety and defensive reactivity: women higher in trait anxiety showed a predominantly accelerative CDR pattern, but anxiety scores were unrelated to the typical CDR pattern found in men. This finding suggests that vulnerability to anxiety disorders involves a gender-specific differential cardiac reactivity to aversive cues, mainly mediated by increased dominance of the sympathetic branch of the autonomic nervous system, and characterized by a more intense, prompter, and durable defensive response for high-anxious women. Specifically, women with higher levels of trait anxiety showed an attenuated early cardiac deceleration and, as hypothesized, a pronounced second accelerative component of the CDR that was also extended in time — consistent with the classic pattern of reciprocal sympathetic
Table 2 Summary of simple regression analyses for CDR medians, using STAI-T scores as predictor, for women (n = 42). Median M1 M2 M3 M4 M5 M6 M7 M8 M9 M10
β
R2
t
p
.16 .25 .33 .45 .44 .52 .45 .43 .40 .45
.03 .06 .11 .20 .19 .27 .20 .18 .16 .21
1.02 1.61 2.22 3.15 3.09 3.84 3.17 2.98 2.74 3.22
.313 .115 .032 .003 .004 b.001 .003 .005 .009 .003
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Fig. 1. Cardiac defense response patterns for women in the High and Low Anxiety groups.
activation and parasympathetic deactivation for anxiety (cf. Kreibig, 2010). Indeed, high-anxious women lacked a true deceleration in the CDR — since HR did not return to baseline levels after the initial acceleration —, suggesting a minimized attentional orienting response towards unexpected, aversive stimuli (i.e., a reduced parasympathetic dominance), and a maximized motivational component of the defensive response (i.e., an increased sympathetic dominance). Additionally, differences associated with trait anxiety lasted throughout the late decelerative component, with a slow return to baseline of cardiac activity in the absence of an actual danger in high-anxious women. Remarkably, high-anxious women showed a first accelerative component commensurate with that of low-anxious women, indicating that this parasympathetic withdrawal-mediated component of the CDR — an index of sensory rejection — does not depend on individual differences in trait anxiety. Conversely, results do suggest a greater predominance of sympathetic vs. parasympathetic activation and a more reactive defensive system in women as a function of increasing dispositional anxiety, consistent with other studies examining the CDR in women with excessive worry (Delgado et al., 2009) or post-traumatic stress disorder (Schalinski et al., 2013). Our results show that, in women alone, anxiety is related to a variation in the temporal course of the defense cascade — that usually begins with an attentional phase followed by a motivational/emotional phase (Lang et al., 1997). It might be possible that the preexisting anxiety state contributes to decrease the threshold for activating the defensive motivational system and to potentiate the coping response to the aversive stimulation, thus diminishing the attentional orienting phase and increasing the motivational components of the defensive reaction in terms of intensity, immediacy and duration (cf. Vila et al., 2007). Beyond, by considering hyperreactivity of the defensive motivational system as a vulnerability factor towards pathological anxiety, our findings seem consistent with prevalence indexes reporting higher proneness to anxiety disorders in women as compared to men (Bruce et al., 2005). Moreover, they add empirical support to the notion of gender-specific associations of clinical anxiety and anxiety vulnerability markers with autonomic hyperreactivity in response to stress (Carrillo et al., 2001; Grossman et al., 2001) and with reductions in autonomic cardiac control as indexed by heart rate variability (Alvares et al., 2013) and, more broadly, to increasing evidence about gender-specific associations in anxiety research across different populations, paradigms, and measures. Thus, gender differences in startle abnormalities have been found in high-risk children (i.e., with a parental history of anxiety disorders) — enhanced fear-potentiated startle in high-risk boys, increased baseline startle in high-risk girls —, suggesting that the vulnerability to anxiety involves a gender-specific differential sensitivity of fear/anxiety pathways (Grillon, Dierker, & Merikangas, 1998). In an event-related brain potentials study about attentional bias in anxiety, anxious women, but not anxious men, displayed greater early visual processing (larger P100 amplitude) to emotional words (Sass et al., 2010). In addition, in a positron emission tomography study, harm avoidance — an anxiety-related personality trait — was negatively correlated with glucose metabolism in the anterior portion of the
ventromedial prefrontal cortex in females but not in males, which suggested gender differences in the association between trait anxiety and autobiographical memory specificity (Hakamata et al., 2009). Selfreported emotion dysregulation plays a greater role in relation to anxiety in girls than it does in boys (Bender, Reinholdt-Dunne, Esbjørn, & Pons, 2012). Finally, high trait anxiety has been directly related to impaired decision-making only in women (de Visser et al., 2010). Overall, these results strongly suggest the existence of a specific phenotypic expression of anxiety in females. At a methodological level, this investigation underscores the utility of the CDR as an indicator of defensive motivational system hyperreactivity in women with a dispositional proneness to react anxiously. Interestingly, our study shows that the effects of high trait anxiety on enhanced cardiovascular response to aversive stimulation can be found at a subclinical level, at least in women. This result is aligned with a dimensional conceptualization of anxiety and supports the appropriateness of studying nonclinical individuals under anxietyprovoking conditions (see Edgar et al., 2007). Notwithstanding this, it would be worthwhile to explore gender-specific endophenotypes of anxiety at clinical levels, using other measures of defensive reactivity (e.g., startle response), in order to clarify the nature and physiological correlates of this broad construct and to help polishing diagnostic and treatment strategies.
Acknowledgments This study was supported by Grant PSI2011-22559 from the Ministerio de Economía y Competitividad (Spain).
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