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Gender differences in the association between psychopathic personality traits and cortisol response to induced stress
ARTICLE IN PRESS Psychoneuroendocrinology (2007) 32, 183–191
Available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/psyneuen
Gender differences in the association between psychopathic personality traits and cortisol response to induced stress Megan M. O’Leary, Bryan R. Loney, Lisa A. Eckel Department of Psychology, Florida State University, Tallahassee, FL 32306-1270, USA Received 28 June 2006; received in revised form 1 December 2006; accepted 8 December 2006
KEYWORDS Psychopathy; Cortisol; Stress; Gender; TSST
Summary Blunted stress reactivity has been implicated in the development of psychopathic personality traits. Cortisol is a biological marker of stress reactivity that has received little attention in prior psychopathy studies. The current investigation proposed that inhibition of cortisol response to induced stress is a reliable marker for psychopathic personality traits. An extreme groups methodology was used to recruit a mixed-gender sample of 84 college students characterized by high and low scores on the Levenson Self-Report Psychopathy Scale. Participants provided saliva samples prior to and after a wellestablished stress induction procedure (i.e., Trier Social Stress Test). These samples were assessed for cortisol (mg/dL) using an enzyme immunoassay procedure. Consistent with prediction, male participants high in psychopathic personality traits lacked stress induced increases in cortisol displayed by males low in psychopathic personality traits. This effect was not present in female participants. These findings suggest that cortisol production is a gender-specific marker for psychopathic personality traits. & 2007 Elsevier Ltd. All rights reserved.
1. Introduction Psychopathic personality traits are the hallmark affective (e.g., shallow emotions) and interpersonal qualities (e.g., callous misuse of others for personal gain) that have historically differentiated a subset of antisocial individuals Corresponding author. Tel.: +1 850 644 1700;
fax: +1 850 644 7739. E-mail address: [email protected] (B.R. Loney). 0306-4530/$ - see front matter & 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.psyneuen.2006.12.004
with the most severe forms of aggression and high levels of criminal recidivism (Hare et al., 1991; Frick et al., 2003; Walters, 2003). These traits are traditionally known as ‘‘Factor I’’ features of the psychopathy construct and are assessed reliably across clinic-referred, forensic, and nonreferred samples (Hare, 2003; Lilienfeld and Widows, 2005). Research consistently documents an association between psychopathic personality traits and pronounced impairment in emotional (or stress) reactivity. For example, psychopathic personality traits have demonstrated a unique association to slowed recognition of distressing words and
ARTICLE IN PRESS 184 pictures (Kimonis et al., 2006; Loney et al., 2003), as well as autonomic nervous system irregularities such as blunted eye blink startle and electrodermal activity (EDA) in response to discrete experimental stressors (e.g., noise blast) (Fung et al., 2005; Lorber, 2004; Patrick, 1994; Raine, 1993). Research suggests that this emotional under-reactivity disrupts fear conditioning and the socialization of conscience and behavioral control (Lykken, 1995; Kochanska, 1997; Blair, 1999). It is important to indicate that psychopathy is a multidimensional construct with separate personality and behavioral features. The behavioral features generally refer to an impulsive and antisocial lifestyle and have traditionally been labeled ‘‘Factor II’’ features.1 While prior research reveals a significant association between psychopathic personality traits (‘‘Factor I’’) and psychopathic behavioral features (‘‘Factor II’’) (e.g., r ¼ .50; Hare et al., 1991; Harpur et al., 1989; Patrick, 1994), there is growing evidence that psychopathic personality traits can occur in the absence of antisocial behavior (Frick et al., 2000; Levenson et al., 1995; Lilienfeld and Andrews, 1996) and most displays of antisocial behavior are not accompanied by psychopathic personality traits (Lykken, 1995; Hare, 1994). In terms of stress reactivity, psychopathic personality traits have demonstrated associations with blunted stress reactivity whether or not accompanied by antisocial behavioral features (Blair, 1999; Frick et al., 2003; Loney et al., 2006). Stress reactivity subsumes various cognitive (e.g., attention to threat stimuli), emotional (e.g., anxiety response), behavioral (e.g., avoidance), and psychophysiological responses (e.g., increased heart rate and general autonomic nervous system activity), and it has been assessed using a wide variety of methods. However, the most reliable and well established stress reactivity effects have been documented for eye blink startle to distressing pictures and EDA in anticipation of noise blast. Nevertheless, the magnitude of these effects are generally modest (i.e., small-tomoderate effect sizes), and this could be attributed to a number of factors including the fact that EDA and related ANS markers are non-specific biological markers of emotional arousal (Bradley, 2000; Herpertz et al., 2001). Additionally, these measures typically focus exclusively on initial reactivity to fear cues that are presented for a brief amount of time (o10 s). This may prove to be a less reliable and potent marker of emotional reactivity than alternative biological measures (e.g., neuroendocrine markers) that are sensitive to the cumulative effects of continued exposure to aversive stimuli. Recently, Loney and colleagues (2006) argued that cortisol production is a promising biological marker of stress reactivity that has been overlooked in prior research on psychopathic personality traits. Although others have 1 Although impulsivity could arguably be viewed as a personality feature, multi-dimensional conceptualizations of psychopathy have generally assigned impulsivity to a behavioral or antisocial lifestyle dimension given that impulsivity has clustered with antisocial behavioral features in many prior factor analytic studies (e.g., Blair et al., 2005; Hare et al., 1991; Harpur et al., 1989; Levenson et al., 1995). However, more importantly, impulsivity is a robust and strong correlate of antisocial behavior that lacks specificity to the psychopathic personality (Frick, 1998; Lilienfeld, 1994).
M.M. O’Leary et al. suggested the need for such research (e.g., van Honk et al., 2003), detailed theoretical modeling and published research findings are lacking. Cortisol is a glucocorticoid hormone that is a peripheral measure of hypothalamic–pituitary–adrenal (HPA) axis activity (Takai et al., 2004). The HPA axis is a well established stress reactivity network that connects the central nervous and endocrine systems (Kudielka and Kirschbaum, 2005). Activation of the HPA axis is triggered by novel/threatening stimuli, which rapidly trigger the release of cortisol from the adrenal cortex into the blood and saliva. Several studies have documented an association between low cortisol production and aggressive behavior (Netter et al., 1999; Pajer et al., 2001). However, other research suggests that cortisol production may only be a marker for the most stable and severe forms of aggressive behavior (McBurnett et al., 2000). Interestingly, low cortisol production is also associated with elevated sensation seeking (Rosenblitt et al., 2002), impaired fear reactivity (Kagan et al., 1988), and the activation of specific brain regions (i.e., the amygdala and orbitofrontal/ventromedial prefrontal cortex) implicated in prior research on psychopathic personality traits (King et al., 2006). Based on these findings, Loney and colleagues (2006) hypothesized that low cortisol is a biological marker for psychopathic personality traits. These researchers recruited a mixed-gender adolescent sample with various combinations of psychopathic personality traits and conduct problems. Consistent with prediction, psychopathic personality traits were associated with low resting cortisol production in the early morning (0900 h) regardless of associated level of conduct problems. However, this effect was only present in male participants. Female participants elevated in psychopathic personality traits were not characterized by low cortisol levels. Testosterone levels were also assessed and were unrelated to psychopathic personality traits across male and female participants. Given that the vast majority of research on psychopathy has been conducted on male research participants, this documented gender difference warrants further research investigation. Of note, Holi et al. (2006) recently found additional support for an association between low resting cortisol production and psychopathic personality traits. However, this study focused exclusively on young adult violent male offenders. Loney et al. noted a number of theoretical and methodological considerations for further research in this area that should be addressed prior to concluding that female psychopathic personality traits are associated with different underlying hormonal activity. This is particularly important given evidence that male and female psychopathic personality traits are similarly related to inhibited eye blink startle to distressing pictures (e.g., Sutton et al., 2002). One limitation of the Loney et al. study was the lack of control for phase of the menstrual cycle in female participants. This could have influenced the results given that the menstrual cycle can influence cortisol levels. Women in the luteal phase (12–14 days before menstruation) are more comparable to males in terms of overall cortisol production. Women in the follicular phase (the more variable interval from cessation of menses to the start of the periovulatory period) and/or on oral contraceptives display significantly lower and restricted cortisol levels (Kirschbaum et al., 1993, 1999). Another limitation that is not unique to
ARTICLE IN PRESS Cortisol and psychopathic personality traits the Loney et al. study was an exclusive focus on resting levels of cortisol production. Prior research on psychopathy and aggressive behavior has used a variety of cortisol sampling methodologies with limited discussion of the potential strengths and weaknesses associated with different approaches (e.g., resting versus stress-induced; morning versus mid-afternoon assessment). Incidentally, different sampling strategies may arguably be tapping distinct neurobiological processes. The vast majority of this research has focused almost exclusively on resting cortisol samples (e.g., McBurnett et al., 2000; van Goozen et al., 1998; Virkkunen, 1985; Holi et al., 2006), and this is arguably an imprecise measure of stress reactivity. Resting cortisol provides an index of general activation of the HPA axis, but change in cortisol production in response to an experimental stressor is a more precise and direct measure of stress reactivity. The assessment of pre-/post-stress changes in cortisol also provides more rigorous control for individual differences in resting cortisol related to time of sampling and related personality and daily living variables. Notably, research suggests that morning assessment is optimal for comparisons of resting cortisol, while afternoon assessment is optimal for comparisons of stress-induced changes. Cortisol peaks in the early morning which may potentiate group differences in resting levels. In contrast, the mid-afternoon is characterized by lower and more variable levels of cortisol makes it easier to capture individual differences in the stress response (Yehuda et al., 2003; Kudielka et al., 2004). The current study was designed to address the aforementioned limitations and to further assess for potential gender differences in the association between psychopathic personality traits and cortisol production. Study participants were assessed first for resting mid-afternoon cortisol activity and then re-assessed for cortisol activity following a stress induction. This is the first published study of the association between psychopathic personality traits and stress induced changes in cortisol production to the researchers’ knowledge. Female cortisol sampling took place exclusively in the luteal phase of the menstrual cycle, and female participants who were currently taking oral contraceptives were excluded from the study. The change in cortisol following the stress induction was the primary variable of interest in the current investigation. It was predicted that participants elevated in psychopathic personality traits would fail to display stress induced increases in cortisol production characteristic of comparison participants. Gender differences were not anticipated given the rigorous control of variables that may have contributed to gender differences in the prior Loney et al. investigation. Finally, the current study was also careful to examine and potentially control for group differences in self-reported anxiety, as cortisol has also been hypothesized by some researchers to be a marker for anxiety (Brown et al., 1996).
2. Method 2.1. Participants A mixed-gender sample of college students (41 males and 43 females) were recruited based on preliminary responses to
185 the Primary Psychopathy subscale of the Levenson SelfReport Psychopathy Scale. This rating scale was administered during a mass screening of psychology students enrolled at a large university in the southeastern United States. A total of 1436 students participated in the screening which included multiple rating scales used to screen and recruit students for additional research projects. Scores on the Primary Psychopathy subscale were used to recruit a similar number of male and female participants from the upper quartile (high psychopathic personality traits: 21 males/22 females) and lower quartile (low psychopathic personality traits: 20 males/21 females) of the screening sample. Recruited participants were predominately European-American (63% European-American, 14% African American, 23% other).
2.2. Measures 2.2.1. Psychopathic personality traits These were assessed using the Levenson Self-Report Psychopathy Scale (SRPS) (Levenson et al., 1995). The SRPS is a 26-item rating scale that contains a 16-item Primary Psychopathy subscale assessing the hallmark psychopathic personality traits that differentiate psychopathy from more general displays of antisocial behavior (e.g., ‘‘I enjoy manipulating other people’s feelings’’ and ‘‘I do not feel bad if my words or actions cause someone else to feel pain’’) (Cleckley, 1976; Hare et al., 1991). Participants in the mass screening were initially divided into high and low psychopathic trait groups based on within-gender upper and lower quartile designations on this subscale. Items on the SRPS are rated on a 4-point Likert-type scale, ranging from 1 (‘‘Disagree strongly’’) to 4 (‘‘Agree strongly’’). The upper quartile cut-scores for the psychopathic personality traits subscale were 39 for males and 35 for females; the lower quartile cut-scores were 28 for males and 24 for females. Of note, the SRPS also contains a 10-item Secondary Psychopathy subscale that assesses for impulsive and antisocial behaviors associated with a more general antisocial lifestyle (e.g., ‘‘I find myself in the same kinds of trouble, time after time’’). This subscale was treated as a potential covariate in the main study analyses to assure that documented group differences were uniquely attributable to psychopathic personality traits rather than just associated levels of antisocial behavior. The SRPS has demonstrated good reliability and validity in previous research using similar non-referred and college samples (e.g., Levenson et al., 1995; Lynam et al., 1999). 2.2.2. Stress induction This was conducted using the Trier Social Stress Test (TSST) (Kirschbaum et al., 1993). The TSST is one of the most prominent and well validated stress induction measures used in prior hormone research (Gaab et al., 2003; Kirschbaum et al., 1993). All TSST sessions were administered by a female experimenter accompanied by mixedgender confederates. In accordance with standard TSST procedures, participants started with a 10 min timed relaxation period prior to providing a pre-stress hormone sample. Participants than immediately participated in a 10 min timed preparation period and 5 min timed mock job
ARTICLE IN PRESS 186 interview/public speaking task in front of 2–3 confederates described as being trained in behavioral observation. A video camera was present and participants were told that they were being filmed and that the film would be reviewed by an expert in verbal and non-verbal behavior. However, no filming actually took place. After the mock job interview, a 5 min timed calculation task was completed (i.e., counting backwards from 2083 in increments of 13) with confederate feedback. In previous studies, the TSST has been shown to increase cortisol levels and heart rate, two well established indices of emotional reactivity (Kirschbaum et al., 1993; Gaab et al., 2003; Kudielka and Kirschbaum, 2005). 2.2.3. Salivary hormone assessment and enzyme immunoassay procedure Salivary cortisol is a well-established sampling method that avoids the stress inducing effects of blood sampling via venipuncture. It has demonstrated strong associations to serum levels in prior research (Yehuda et al., 2003; Takai et al., 2004; Kudielka and Kirschbaum, 2005). To assess preand post-stress cortisol levels, participants were required to deposit 6 ml of saliva into two separate collection vials. Consistent with prior research on cortisol response to stress (e.g., Gaab et al., 2003; van Honk et al., 2003), all saliva samples were collected in the mid-afternoon between 1400 and 1800 h. This was done given that cortisol rapidly peaks and displays a constricted range in the morning which can mask underlying group differences in the stress response (Kudielka et al., 2004). Participants were required to abstain from exercise, smoking, eating, and consuming caffeinated beverages or alcohol for 1 h prior to the study, as these variables have been shown to impact cortisol production (Takai et al., 2004). Females were also scheduled to come in during the 12–14 days preceding menstruation and were excluded from participation if currently taking an oral contraceptive. Additionally, all participants were asked to indicate any additional prescription and non-prescription medications they were currently taking or had taken in the last 2 weeks. No participants were taking medications with well documented effects on cortisol production including beta blockers, glucocorticoids, and estrogens (Handa et al., 1994). Only 18% of the sample reported any medication use with the most common medications being topical acne and allergy medications. Saliva samples were frozen at 20 1C until assayed. Upon completion of data collection, the samples were shipped on dry ice to a company specializing in the assessment of salivary cortisol (i.e., Salimetrics, State College, PA). Salimetrics conducted the assays using an enzyme immunoassay procedure. All samples were assayed for cortisol (mg/dL) in duplicate, and the average of duplicate tests was used in analyses. The lower limit of sensitivity was o.003 mg/dL, and the intra-assay coefficients of variations for the pre-stress and post-stress cortisol assays were 4.49 and 3.88, respectively. 2.2.4. Anxiety Trait anxiety was assessed using the 20-item trait anxiety scale from the State-Trait Anxiety Inventory (Spielberger, 1983). Items are rated on a 4-point Likert scale with responses ranging from ‘‘1 ¼ almost never’’ to ‘‘4 ¼ almost
M.M. O’Leary et al. always’’ (e.g., ‘‘I worry too much over something that really doesn’t matter’’ and ‘‘I feel that difficulties are piling up so that I cannot overcome them’’). This is a well-established anxiety measure with strong psychometric properties (Barnes et al., 2002).
2.3. Procedure All participants were contacted by phone and asked if they would like to participate in the research project. At this time, participants were asked to refrain from exercise, smoking, eating, and consuming caffeinated beverages or alcohol for 1 h prior to their participation. Additionally, female participants were asked when their last menstrual cycle ended, and they were scheduled to be tested at least 2 weeks from that day and prior to the onset of menstruation. All procedures were carried out with adequate understanding and written consent of study participants. Upon arrival to the research lab, participants first read and signed a consent form. They then completed a brief questionnaire that confirmed compliance with the eating, drinking, exercise, and menstrual cycle restrictions. To maintain the integrity of the stress manipulation, participants were informed that they were participating in a study assessing the relation between hormone functioning, personality styles, and job performance. The TSST was then administered. Immediately following the 10 min TSST relaxation period, participants provided a pre-stress saliva sample. They then provided a second saliva sample immediately following the completion of the TSST. Twenty minutes separated hormone assessments for all participants. Finally, participants completed the anxiety measure. All participants were debriefed and received course credit for their participation.
3. Results Table 1 provides descriptive statistics for the recruited participants by gender and level of psychopathic personality traits. As expected for a non-referred sample, the participants were generally characterized by relatively low levels of anxiety.2 Because the groups did not differ significantly in anxiety, this measure was not used as a covariate in subsequent group comparisons.3 A comparison of psychopathy scores across groups supported the integrity of group formation. Overall, the groups significantly differed on Levenson Primary Psychopathy (i.e., psychopathic personality traits) scores with subsequent pairwise comparisons indicating that male and female groups characterized by high psychopathic personality traits were appropriately higher in psychopathic personality traits than comparison 2 Due to data collection error, anxiety data were missing for one participant in the male group characterized by low psychopathic personality traits. A mean imputation method was used to replace this participant’s anxiety score with the overall sample mean for the variable. 3 Further examination of anxiety scores revealed a non-significant association to both pre-stress, r ¼ .02, p ¼ ns, and post-stress cortisol levels, r ¼ .19, p ¼ ns. Additionally, introducing anxiety as a covariate in the main group analyses did not alter the pattern or magnitude of findings.
ARTICLE IN PRESS Cortisol and psychopathic personality traits
Table 1
187
Sample descriptive statistics and group comparisons. Male participants
Age (SD) Anxiety (SD) Levenson Psychopathy Scale Primary psychopathy (SD) Secondary psychopathy (SD)
Female participants
Low psychopathic personality traits (n ¼ 20)
High psychopathic personality traits (n ¼ 21)
Low psychopathic personality traits (n ¼ 21)
High psychopathic personality traits (n ¼ 22)
F
18.52 (1.05) 34.82 (6.79)
18.50 (0.83) 36.00 (9.29)
18.38 (0.80) 37.67 (10.94)
18.50 (1.14) 39.27 (10.58)
.31 .88
23.75a (3.97) 18.35a (2.52)
42.61b (4.51) 24.49b (3.85)
20.76a (2.59) 17.40a (4.56)
39.59b (4.31) 22.60b (5.63)
165.86** 12.80**
(3,80)
X 2ð3;N¼84Þ Ethnicity (% Minority)
55%
a
29%
ab
14%
b
50%
a
9.67*
Note: Means with different subscripts were significantly different (po.05) in pairwise comparisons using the Chi square test for the ethnicity variable and the Tukey’s HSD test for all other variables. *po.05 and **po.001.
groups. Additionally, male and female groups with similar designations (e.g., low or high psychopathic personality traits) did not differ significantly in level of psychopathic personality traits. This removed the possibility that any documented gender differences could be accounted for by differing levels of psychopathic personality traits. Analogous results were found for Levenson Secondary Psychopathy scores (i.e., psychopathic behavioral features). The groups did differ significantly in percentage of minority participants. Males characterized by low psychopathic personality traits and females characterized by high psychopathic personality traits had a significantly greater percentage of minority participants than females low in psychopathic personality traits.4 In order to test the main study hypotheses, a 2*2*2 mixeddesign ANOVA was conducted, with group status (low or high psychopathic personality traits) and gender as betweensubjects variables, and time of saliva sample (pre-stress and post-stress) as a within-subjects variable. Of note, the observed range of pre-stress (M ¼ .27 mg/dL, SD ¼ .14, range ¼ .07–.85) and post-stress cortisol levels (M ¼ .41 mg/dL, SD ¼ .27, range ¼ .10–1.62) were within normal parameters for the demographic characteristics of the sample (e.g., Habra et al., 2003; Kudielka et al., 2004). None of the cortisol values were outside of established parameters within and across the recruited groups. The ANOVA revealed a significant 3-way interaction, F (1,80) ¼ 9.73, po0.05, that qualified any assertions that could be made about main effects. These analyses were also conducted introducing Levenson SRPS Secondary Psychopathy scores as a covariate. This was done to assure that documented group differences were uniquely related to 4
Ethnicity information was presented strictly for descriptive purposes. Although no a priori hypotheses were made concerning ethnicity, minority status displayed non-significant associations to pre-stress, t (82) ¼ 1.41, p ¼ ns, and post-stress cortisol levels, t (82) ¼ 0.04, p ¼ ns. Furthermore, introducing minority status as a covariate in the main group analyses did not alter the pattern or magnitude of findings.
psychopathic personality traits rather than covarying levels of psychopathic behavioral features (i.e., impulsive and antisocial behavior) tapped by the Secondary Psychopathy subscale. A preliminary analysis revealed non-significant bivariate associations between the Secondary Psychopathy subscale and both pre-stress, r ¼ .05, p ¼ ns, and post-stress cortisol levels, r ¼ .14, p ¼ ns. Further, the introduction of this covariate did not alter the pattern or magnitude of the reported findings. Fig. 1 provides a graphical representation of the threeway interaction. While psychopathic personality traits moderated cortisol response to the stress induction, this effect was limited to the male participants. Consistent with prediction, pairwise comparisons confirmed that males low in psychopathic personality traits exhibited a statistically significant increase in cortisol following the stress induction, po.001, that was lacking for the males elevated in psychopathic personality traits, p ¼ .21. Importantly, male recruitment groups did not differ significantly in pre-stress cortisol levels, p ¼ .99. A comparison of the average increase in cortisol following the stress induction (poststress minus pre-stress cortisol) for males low in psychopathic personality traits (M ¼ .35, SD ¼ .30) and high in psychopathic personality traits (M ¼ .10, SD ¼ .13) revealed a large effect size, d ¼ 1.08 (Cohen, 1992). Female recruitment groups did not differ significantly on pre-stress, p ¼ .99, or post-stress cortisol levels, p ¼ .99. Furthermore, both female groups failed to display significant increases in cortisol in response to the stress induction, p values 4.82.
4. Discussion The current study replicates and extends the recent Loney et al. (2006) report that cortisol production is a biological marker for male psychopathic personality traits. Male participants characterized by elevations in psychopathic personality traits failed to display stress induced increases in cortisol that were present for males low in psychopathic personality traits. This was a large effect (d ¼ 1.08) that
ARTICLE IN PRESS 188
M.M. O’Leary et al.
0.9
males
females
0.8
* low psychopathic traits
salivary cortisol (µg/dl)
0.7
high psychopathic traits
0.6 0.5 0.4 0.3 0.2 0.1
pre
post stress induction
pre
post stress induction
Figure 1 Average pre- and post-stress salivary cortisol levels (mg/dL) by group and gender. As predicted, males low in psychopathic personality traits displayed a significant increase in cortisol relative to comparison groups. Females displayed nominal and nonsignificant increases in cortisol across recruitment groups. *Greater than both the male low psychopathic personality traits/pre-stress condition, po.001, and the male high psychopathic personality traits/post-stress condition, po.01.
was only present for the male participants. Female participants failed to display increases in cortisol following the stress induction regardless of the level of psychopathic personality traits. For males, it was interesting that no differences in prestress (or resting) cortisol levels were documented given that Loney et al. (2006) focused exclusively on resting cortisol and found that male psychopathic personality traits were associated with low resting cortisol. Nevertheless, it is important to reiterate that the Loney et al. study sampled cortisol in the early morning and the current study sampled cortisol in the mid-afternoon. Given the diurnal variability of cortisol production (i.e., peaks and less variability in the morning; stabilizes and more variable in the mid-afternoon), differences in resting cortisol effects are not surprising. After all, morning sampling is generally recommended for comparisons of resting cortisol and mid-afternoon assessments are generally recommended for the assessment of stress-induced changes (Kudielka et al., 2004). Regardless, Loney et al. suggested that resting cortisol may also be a less reliable and valid indicator of stress reactivity given the multitude of daily living factors that can impact resting cortisol levels and the failure to directly assess biological reactivity to a threat stimulus. The current study rigorously controlled for daily living variables that were not controlled for in the Loney et al. study (e.g., recent exercise and smoking) and also contained older participants. Future research should continue to assess the reliability of resting cortisol effects across distinct time periods (e.g., morning and mid-afternoon), particularly given that indicators of resting autonomic nervous system activity (e.g., low resting heart rate) have proven to be reliable markers of psychopathic personality traits (Raine, 2002). However, the assessment of stress-induced changes in cortisol is arguably
a more precise measure of stress reactivity that has the benefit of gauging cumulative biological reactivity to a wide variety of threat stimuli. Stress induced changes also provide more rigorous control for individual differences in resting cortisol related to developmental level and related personality and daily living variables. Methodologically, this could make this measure and associated findings more robust to age and setting of participants. Females elevated in psychopathic personality traits responded as expected and similarly to males elevated in psychopathic personality traits. Perhaps the more intriguing finding was the lack of stress-induced increase in cortisol for female participants characterized by low psychopathic personality traits. The failure of the stress induction to elicit increases in cortisol for the female control participants suggests some important methodological and theoretical considerations for future research. First, it is possible that sociocultural influences are operating to shape sensitivity to the stress induction. While prior research with the TSST has generally produced cortisol responses in males and females (Dickerson and Kemeny, 2004), there is evidence that gender is associated with differences in subjective interpretation of stressful events and related psychobiological responsiveness to stress stimuli (e.g., Kudielka and Kirschbaum, 2005; Stroud et al., 2002). Furthermore, some other recent TSST research has suggested that male salivary cortisol response is greater than female salivary cortisol response (e.g., Kudielka and Kirschbaum, 2005), and this mirrors other recent findings suggesting that higher salivary cortisol responses are found in young men after exposure to acute real-life and laboratory psychological stressors (i.e. academic exams, free speech, mental arithmetic) (Stroud et al., 2002; Kajantie and Phillips, 2006). This suggests that future research will need to carefully consider the nature of
ARTICLE IN PRESS Cortisol and psychopathic personality traits threat stimuli used in psychopathy investigations prior to determining if null effects provide robust evidence that cortisol irregularities are not present for female participants. Young women are generally socialized for a relational orientation by authority figures and peers, and this is contrasted with a sociocultural emphasis on instrumentality and physical dominance for young men (Crick and ZahnWaxler, 2003). Interestingly, the TSST contains a performance-based threat that is arguably more sensitive to an instrumental orientation. Future research should integrate stress induction measures that tap a relational orientation, such as peer rejection paradigm, in order to further examine if sociocultural influences may account in part for the documented findings (cf. Stroud et al., 2002). Prior psychopathy research has largely focused on male participants and has therefore generally failed to discuss the impact of gender socialization on the emotional underreactivity implicated in dominant etiological models. Future research could benefit from more detailed biopsychosocial modeling that accounts for the role of gender socialization in the development and expression of psychopathic personality traits. This has implications for future hormone investigations, but it may also prove useful in other related cognitive and behavioral studies. For example, there is now evidence that females and males elevated in psychopathic personality traits display similarly attenuated eye blink startle to distressing pictures such as body mutilations (Sutton et al., 2002). However, there is also evidence that females elevated in psychopathic personality traits lack hypersensitivity to cues for reward (i.e., reward dominance) that is present for males elevated in psychopathic personality traits (Vitale and Newman, 2001). Similar to the current hormone findings, these prior findings could also be explained by gender socialization practices as indices of reward dominance are more sensitive to an instrumental orientation. Related considerations for future research pertain to the assessment of menstrual cycle and the gender of experimenter conducting the stress manipulations. Although the current study followed a protocol consistent with other research examining menstrual cycle phase through self report (e.g., Smeets et al., 2006), this method is less reliable than biological verification of menstrual phase. Future research should consider directly assessing progesterone levels to verify luteal phase assessment. During the luteal phase, mean salivary progesterone increases dramatically with an average concentration of 300 pg/ml (range ¼ 100–500 pg/ml) (White et al., 2002). Any female participants with salivary progesterone levels less than 100 pg/ml could be excluded or treated separately in analyses. Additionally, future research should consider systematically investigating the impact of experimenter gender on study findings. The current study relied exclusively on female experimenters (for males and females), and this may assist in explaining the female findings given that opposite-gender experimenters could increase the impact of the stress induction. The use of opposite-sex experimenters for female participants could further clarify whether experimenter gender accounts in part for the lack of female findings. The current findings must be interpreted in the context of the following limitations. First, the findings were derived on
189 a regionally bound college sample, and the phone call recruitment methodology could have introduced some selfselection biases. Future research should attempt to replicate the study findings in more diverse samples, particularly given that the study of psychopathic personality traits is often conducted in prison settings. Nevertheless, numerous studies have established the reliability and validity of psychopathic personality traits in non-referred and college-aged samples (e.g., Levenson et al., 1995; Lilienfeld and Andrews, 1996; Frick et al., 2003). Furthermore, the use of a non-referred sample removed the potential confound of prison exposure and accumulating antisocial histories present in many prior psychopathy studies. A separate limitation pertains to the extreme groups recruitment approach. The sampling of participants at the upper and lower ends of the distribution of psychopathic traits is commonly done in non-referred psychopathy studies given evidence that psychopathic traits are non-normally distributed and potentially taxonic in nature (Harris et al., 1994; Vasey et al., 2005). Incidentally, the use of this strategy in the current study resulted in SRPS for males/ females in the high psychopathic personality traits groups that were quite comparable to prior prison-based psychopathy research (Brinkley et al., 2001). Extreme groups recruitment is generally recommended for nascent and exploratory research areas such as the current study focus to assist with detecting trends and guiding future studies (Preacher et al., 2005). Nevertheless, as this research area develops, it could be informative to sample at the middle of the distribution to further explore whether psychopathic traits display linear or non-linear associations to cortisol production. Beyond these sampling and recruitment concerns, the current study only sampled cortisol across two time points. This leaves open the possibility that male psychopathic personality traits are associated with greater latency to a cortisol response rather than an absence of a cortisol response. A common methodology for assessing cortisol that has not been used in the study of psychopathic personality traits and aggression is to take repeated saliva samples in 20 min intervals across a 1 1 12 h testing session. This allows for the assessment of changes in cortisol from baseline to peak cortisol response and subsequent recovery (e.g., Dickerson and Kemeny, 2004; Kirschbaum et al., 1993; Kudielka and Kirschbaum, 2005). The integration of this cortisol methodology could allow for detection of group differences in both the initial stress response as well as recovery of the stress response. It would also assist in rulingout the possibility of latency effects (e.g., delayed rather than lack of cortisol response to stressor). Finally, the current study relied exclusively on one measure of emotional reactivity. As mentioned above, future research should expand the nature of the stress stimuli used in cortisol investigations (e.g., performance versus social threat). However, it would also be beneficial to integrate related laboratory and performance-based measures (e.g., electrodermal activity and eye blink startle measures) that ostensibly measure similar emotional reactivity processes. Emotional reactivity subsumes multiple cognitive (e.g., orientation of attention and cognitive appraisal), behavioral (e.g., fight/flight responses), and physiological (e.g., accelerated heart rate and increased
ARTICLE IN PRESS 190 HPA-axis activity) processes that may vary as a function of sociocultural influences. Directly assessing the association between cortisol and related emotional reactivity indices could greatly assist in discerning the specific processes related to male and female psychopathic personality traits. This type of research should also be sensitive to the increasing specificity of brain regions implicated in the development of psychopathic personality traits (King et al., 2006). In summary, the current findings provide increasing support for the hypothesis that cortisol production is a biological marker for male psychopathic personality traits. With continued replication, this type of research has the potential to enhance etiological modeling through greater specificity of putative biological risk variables (i.e., blunted reactivity of the HPA-axis). Furthermore, it suggests a relatively easy and non-invasive method of assessing emotional reactivity that could potentially be used to gauge impairment levels and associated response to psychosocial treatment for males elevated in psychopathic personality traits.
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Gender differences in the association between psychopathic personality traits and cortisol response to induced stress Megan M. O’Leary, Bryan R. Loney, Lisa A. Eckel Department of Psychology, Florida State University, Tallahassee, FL 32306-1270, USA Received 28 June 2006; received in revised form 1 December 2006; accepted 8 December 2006
KEYWORDS Psychopathy; Cortisol; Stress; Gender; TSST
Summary Blunted stress reactivity has been implicated in the development of psychopathic personality traits. Cortisol is a biological marker of stress reactivity that has received little attention in prior psychopathy studies. The current investigation proposed that inhibition of cortisol response to induced stress is a reliable marker for psychopathic personality traits. An extreme groups methodology was used to recruit a mixed-gender sample of 84 college students characterized by high and low scores on the Levenson Self-Report Psychopathy Scale. Participants provided saliva samples prior to and after a wellestablished stress induction procedure (i.e., Trier Social Stress Test). These samples were assessed for cortisol (mg/dL) using an enzyme immunoassay procedure. Consistent with prediction, male participants high in psychopathic personality traits lacked stress induced increases in cortisol displayed by males low in psychopathic personality traits. This effect was not present in female participants. These findings suggest that cortisol production is a gender-specific marker for psychopathic personality traits. & 2007 Elsevier Ltd. All rights reserved.
1. Introduction Psychopathic personality traits are the hallmark affective (e.g., shallow emotions) and interpersonal qualities (e.g., callous misuse of others for personal gain) that have historically differentiated a subset of antisocial individuals Corresponding author. Tel.: +1 850 644 1700;
fax: +1 850 644 7739. E-mail address: [email protected] (B.R. Loney). 0306-4530/$ - see front matter & 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.psyneuen.2006.12.004
with the most severe forms of aggression and high levels of criminal recidivism (Hare et al., 1991; Frick et al., 2003; Walters, 2003). These traits are traditionally known as ‘‘Factor I’’ features of the psychopathy construct and are assessed reliably across clinic-referred, forensic, and nonreferred samples (Hare, 2003; Lilienfeld and Widows, 2005). Research consistently documents an association between psychopathic personality traits and pronounced impairment in emotional (or stress) reactivity. For example, psychopathic personality traits have demonstrated a unique association to slowed recognition of distressing words and
ARTICLE IN PRESS 184 pictures (Kimonis et al., 2006; Loney et al., 2003), as well as autonomic nervous system irregularities such as blunted eye blink startle and electrodermal activity (EDA) in response to discrete experimental stressors (e.g., noise blast) (Fung et al., 2005; Lorber, 2004; Patrick, 1994; Raine, 1993). Research suggests that this emotional under-reactivity disrupts fear conditioning and the socialization of conscience and behavioral control (Lykken, 1995; Kochanska, 1997; Blair, 1999). It is important to indicate that psychopathy is a multidimensional construct with separate personality and behavioral features. The behavioral features generally refer to an impulsive and antisocial lifestyle and have traditionally been labeled ‘‘Factor II’’ features.1 While prior research reveals a significant association between psychopathic personality traits (‘‘Factor I’’) and psychopathic behavioral features (‘‘Factor II’’) (e.g., r ¼ .50; Hare et al., 1991; Harpur et al., 1989; Patrick, 1994), there is growing evidence that psychopathic personality traits can occur in the absence of antisocial behavior (Frick et al., 2000; Levenson et al., 1995; Lilienfeld and Andrews, 1996) and most displays of antisocial behavior are not accompanied by psychopathic personality traits (Lykken, 1995; Hare, 1994). In terms of stress reactivity, psychopathic personality traits have demonstrated associations with blunted stress reactivity whether or not accompanied by antisocial behavioral features (Blair, 1999; Frick et al., 2003; Loney et al., 2006). Stress reactivity subsumes various cognitive (e.g., attention to threat stimuli), emotional (e.g., anxiety response), behavioral (e.g., avoidance), and psychophysiological responses (e.g., increased heart rate and general autonomic nervous system activity), and it has been assessed using a wide variety of methods. However, the most reliable and well established stress reactivity effects have been documented for eye blink startle to distressing pictures and EDA in anticipation of noise blast. Nevertheless, the magnitude of these effects are generally modest (i.e., small-tomoderate effect sizes), and this could be attributed to a number of factors including the fact that EDA and related ANS markers are non-specific biological markers of emotional arousal (Bradley, 2000; Herpertz et al., 2001). Additionally, these measures typically focus exclusively on initial reactivity to fear cues that are presented for a brief amount of time (o10 s). This may prove to be a less reliable and potent marker of emotional reactivity than alternative biological measures (e.g., neuroendocrine markers) that are sensitive to the cumulative effects of continued exposure to aversive stimuli. Recently, Loney and colleagues (2006) argued that cortisol production is a promising biological marker of stress reactivity that has been overlooked in prior research on psychopathic personality traits. Although others have 1 Although impulsivity could arguably be viewed as a personality feature, multi-dimensional conceptualizations of psychopathy have generally assigned impulsivity to a behavioral or antisocial lifestyle dimension given that impulsivity has clustered with antisocial behavioral features in many prior factor analytic studies (e.g., Blair et al., 2005; Hare et al., 1991; Harpur et al., 1989; Levenson et al., 1995). However, more importantly, impulsivity is a robust and strong correlate of antisocial behavior that lacks specificity to the psychopathic personality (Frick, 1998; Lilienfeld, 1994).
M.M. O’Leary et al. suggested the need for such research (e.g., van Honk et al., 2003), detailed theoretical modeling and published research findings are lacking. Cortisol is a glucocorticoid hormone that is a peripheral measure of hypothalamic–pituitary–adrenal (HPA) axis activity (Takai et al., 2004). The HPA axis is a well established stress reactivity network that connects the central nervous and endocrine systems (Kudielka and Kirschbaum, 2005). Activation of the HPA axis is triggered by novel/threatening stimuli, which rapidly trigger the release of cortisol from the adrenal cortex into the blood and saliva. Several studies have documented an association between low cortisol production and aggressive behavior (Netter et al., 1999; Pajer et al., 2001). However, other research suggests that cortisol production may only be a marker for the most stable and severe forms of aggressive behavior (McBurnett et al., 2000). Interestingly, low cortisol production is also associated with elevated sensation seeking (Rosenblitt et al., 2002), impaired fear reactivity (Kagan et al., 1988), and the activation of specific brain regions (i.e., the amygdala and orbitofrontal/ventromedial prefrontal cortex) implicated in prior research on psychopathic personality traits (King et al., 2006). Based on these findings, Loney and colleagues (2006) hypothesized that low cortisol is a biological marker for psychopathic personality traits. These researchers recruited a mixed-gender adolescent sample with various combinations of psychopathic personality traits and conduct problems. Consistent with prediction, psychopathic personality traits were associated with low resting cortisol production in the early morning (0900 h) regardless of associated level of conduct problems. However, this effect was only present in male participants. Female participants elevated in psychopathic personality traits were not characterized by low cortisol levels. Testosterone levels were also assessed and were unrelated to psychopathic personality traits across male and female participants. Given that the vast majority of research on psychopathy has been conducted on male research participants, this documented gender difference warrants further research investigation. Of note, Holi et al. (2006) recently found additional support for an association between low resting cortisol production and psychopathic personality traits. However, this study focused exclusively on young adult violent male offenders. Loney et al. noted a number of theoretical and methodological considerations for further research in this area that should be addressed prior to concluding that female psychopathic personality traits are associated with different underlying hormonal activity. This is particularly important given evidence that male and female psychopathic personality traits are similarly related to inhibited eye blink startle to distressing pictures (e.g., Sutton et al., 2002). One limitation of the Loney et al. study was the lack of control for phase of the menstrual cycle in female participants. This could have influenced the results given that the menstrual cycle can influence cortisol levels. Women in the luteal phase (12–14 days before menstruation) are more comparable to males in terms of overall cortisol production. Women in the follicular phase (the more variable interval from cessation of menses to the start of the periovulatory period) and/or on oral contraceptives display significantly lower and restricted cortisol levels (Kirschbaum et al., 1993, 1999). Another limitation that is not unique to
ARTICLE IN PRESS Cortisol and psychopathic personality traits the Loney et al. study was an exclusive focus on resting levels of cortisol production. Prior research on psychopathy and aggressive behavior has used a variety of cortisol sampling methodologies with limited discussion of the potential strengths and weaknesses associated with different approaches (e.g., resting versus stress-induced; morning versus mid-afternoon assessment). Incidentally, different sampling strategies may arguably be tapping distinct neurobiological processes. The vast majority of this research has focused almost exclusively on resting cortisol samples (e.g., McBurnett et al., 2000; van Goozen et al., 1998; Virkkunen, 1985; Holi et al., 2006), and this is arguably an imprecise measure of stress reactivity. Resting cortisol provides an index of general activation of the HPA axis, but change in cortisol production in response to an experimental stressor is a more precise and direct measure of stress reactivity. The assessment of pre-/post-stress changes in cortisol also provides more rigorous control for individual differences in resting cortisol related to time of sampling and related personality and daily living variables. Notably, research suggests that morning assessment is optimal for comparisons of resting cortisol, while afternoon assessment is optimal for comparisons of stress-induced changes. Cortisol peaks in the early morning which may potentiate group differences in resting levels. In contrast, the mid-afternoon is characterized by lower and more variable levels of cortisol makes it easier to capture individual differences in the stress response (Yehuda et al., 2003; Kudielka et al., 2004). The current study was designed to address the aforementioned limitations and to further assess for potential gender differences in the association between psychopathic personality traits and cortisol production. Study participants were assessed first for resting mid-afternoon cortisol activity and then re-assessed for cortisol activity following a stress induction. This is the first published study of the association between psychopathic personality traits and stress induced changes in cortisol production to the researchers’ knowledge. Female cortisol sampling took place exclusively in the luteal phase of the menstrual cycle, and female participants who were currently taking oral contraceptives were excluded from the study. The change in cortisol following the stress induction was the primary variable of interest in the current investigation. It was predicted that participants elevated in psychopathic personality traits would fail to display stress induced increases in cortisol production characteristic of comparison participants. Gender differences were not anticipated given the rigorous control of variables that may have contributed to gender differences in the prior Loney et al. investigation. Finally, the current study was also careful to examine and potentially control for group differences in self-reported anxiety, as cortisol has also been hypothesized by some researchers to be a marker for anxiety (Brown et al., 1996).
2. Method 2.1. Participants A mixed-gender sample of college students (41 males and 43 females) were recruited based on preliminary responses to
185 the Primary Psychopathy subscale of the Levenson SelfReport Psychopathy Scale. This rating scale was administered during a mass screening of psychology students enrolled at a large university in the southeastern United States. A total of 1436 students participated in the screening which included multiple rating scales used to screen and recruit students for additional research projects. Scores on the Primary Psychopathy subscale were used to recruit a similar number of male and female participants from the upper quartile (high psychopathic personality traits: 21 males/22 females) and lower quartile (low psychopathic personality traits: 20 males/21 females) of the screening sample. Recruited participants were predominately European-American (63% European-American, 14% African American, 23% other).
2.2. Measures 2.2.1. Psychopathic personality traits These were assessed using the Levenson Self-Report Psychopathy Scale (SRPS) (Levenson et al., 1995). The SRPS is a 26-item rating scale that contains a 16-item Primary Psychopathy subscale assessing the hallmark psychopathic personality traits that differentiate psychopathy from more general displays of antisocial behavior (e.g., ‘‘I enjoy manipulating other people’s feelings’’ and ‘‘I do not feel bad if my words or actions cause someone else to feel pain’’) (Cleckley, 1976; Hare et al., 1991). Participants in the mass screening were initially divided into high and low psychopathic trait groups based on within-gender upper and lower quartile designations on this subscale. Items on the SRPS are rated on a 4-point Likert-type scale, ranging from 1 (‘‘Disagree strongly’’) to 4 (‘‘Agree strongly’’). The upper quartile cut-scores for the psychopathic personality traits subscale were 39 for males and 35 for females; the lower quartile cut-scores were 28 for males and 24 for females. Of note, the SRPS also contains a 10-item Secondary Psychopathy subscale that assesses for impulsive and antisocial behaviors associated with a more general antisocial lifestyle (e.g., ‘‘I find myself in the same kinds of trouble, time after time’’). This subscale was treated as a potential covariate in the main study analyses to assure that documented group differences were uniquely attributable to psychopathic personality traits rather than just associated levels of antisocial behavior. The SRPS has demonstrated good reliability and validity in previous research using similar non-referred and college samples (e.g., Levenson et al., 1995; Lynam et al., 1999). 2.2.2. Stress induction This was conducted using the Trier Social Stress Test (TSST) (Kirschbaum et al., 1993). The TSST is one of the most prominent and well validated stress induction measures used in prior hormone research (Gaab et al., 2003; Kirschbaum et al., 1993). All TSST sessions were administered by a female experimenter accompanied by mixedgender confederates. In accordance with standard TSST procedures, participants started with a 10 min timed relaxation period prior to providing a pre-stress hormone sample. Participants than immediately participated in a 10 min timed preparation period and 5 min timed mock job
ARTICLE IN PRESS 186 interview/public speaking task in front of 2–3 confederates described as being trained in behavioral observation. A video camera was present and participants were told that they were being filmed and that the film would be reviewed by an expert in verbal and non-verbal behavior. However, no filming actually took place. After the mock job interview, a 5 min timed calculation task was completed (i.e., counting backwards from 2083 in increments of 13) with confederate feedback. In previous studies, the TSST has been shown to increase cortisol levels and heart rate, two well established indices of emotional reactivity (Kirschbaum et al., 1993; Gaab et al., 2003; Kudielka and Kirschbaum, 2005). 2.2.3. Salivary hormone assessment and enzyme immunoassay procedure Salivary cortisol is a well-established sampling method that avoids the stress inducing effects of blood sampling via venipuncture. It has demonstrated strong associations to serum levels in prior research (Yehuda et al., 2003; Takai et al., 2004; Kudielka and Kirschbaum, 2005). To assess preand post-stress cortisol levels, participants were required to deposit 6 ml of saliva into two separate collection vials. Consistent with prior research on cortisol response to stress (e.g., Gaab et al., 2003; van Honk et al., 2003), all saliva samples were collected in the mid-afternoon between 1400 and 1800 h. This was done given that cortisol rapidly peaks and displays a constricted range in the morning which can mask underlying group differences in the stress response (Kudielka et al., 2004). Participants were required to abstain from exercise, smoking, eating, and consuming caffeinated beverages or alcohol for 1 h prior to the study, as these variables have been shown to impact cortisol production (Takai et al., 2004). Females were also scheduled to come in during the 12–14 days preceding menstruation and were excluded from participation if currently taking an oral contraceptive. Additionally, all participants were asked to indicate any additional prescription and non-prescription medications they were currently taking or had taken in the last 2 weeks. No participants were taking medications with well documented effects on cortisol production including beta blockers, glucocorticoids, and estrogens (Handa et al., 1994). Only 18% of the sample reported any medication use with the most common medications being topical acne and allergy medications. Saliva samples were frozen at 20 1C until assayed. Upon completion of data collection, the samples were shipped on dry ice to a company specializing in the assessment of salivary cortisol (i.e., Salimetrics, State College, PA). Salimetrics conducted the assays using an enzyme immunoassay procedure. All samples were assayed for cortisol (mg/dL) in duplicate, and the average of duplicate tests was used in analyses. The lower limit of sensitivity was o.003 mg/dL, and the intra-assay coefficients of variations for the pre-stress and post-stress cortisol assays were 4.49 and 3.88, respectively. 2.2.4. Anxiety Trait anxiety was assessed using the 20-item trait anxiety scale from the State-Trait Anxiety Inventory (Spielberger, 1983). Items are rated on a 4-point Likert scale with responses ranging from ‘‘1 ¼ almost never’’ to ‘‘4 ¼ almost
M.M. O’Leary et al. always’’ (e.g., ‘‘I worry too much over something that really doesn’t matter’’ and ‘‘I feel that difficulties are piling up so that I cannot overcome them’’). This is a well-established anxiety measure with strong psychometric properties (Barnes et al., 2002).
2.3. Procedure All participants were contacted by phone and asked if they would like to participate in the research project. At this time, participants were asked to refrain from exercise, smoking, eating, and consuming caffeinated beverages or alcohol for 1 h prior to their participation. Additionally, female participants were asked when their last menstrual cycle ended, and they were scheduled to be tested at least 2 weeks from that day and prior to the onset of menstruation. All procedures were carried out with adequate understanding and written consent of study participants. Upon arrival to the research lab, participants first read and signed a consent form. They then completed a brief questionnaire that confirmed compliance with the eating, drinking, exercise, and menstrual cycle restrictions. To maintain the integrity of the stress manipulation, participants were informed that they were participating in a study assessing the relation between hormone functioning, personality styles, and job performance. The TSST was then administered. Immediately following the 10 min TSST relaxation period, participants provided a pre-stress saliva sample. They then provided a second saliva sample immediately following the completion of the TSST. Twenty minutes separated hormone assessments for all participants. Finally, participants completed the anxiety measure. All participants were debriefed and received course credit for their participation.
3. Results Table 1 provides descriptive statistics for the recruited participants by gender and level of psychopathic personality traits. As expected for a non-referred sample, the participants were generally characterized by relatively low levels of anxiety.2 Because the groups did not differ significantly in anxiety, this measure was not used as a covariate in subsequent group comparisons.3 A comparison of psychopathy scores across groups supported the integrity of group formation. Overall, the groups significantly differed on Levenson Primary Psychopathy (i.e., psychopathic personality traits) scores with subsequent pairwise comparisons indicating that male and female groups characterized by high psychopathic personality traits were appropriately higher in psychopathic personality traits than comparison 2 Due to data collection error, anxiety data were missing for one participant in the male group characterized by low psychopathic personality traits. A mean imputation method was used to replace this participant’s anxiety score with the overall sample mean for the variable. 3 Further examination of anxiety scores revealed a non-significant association to both pre-stress, r ¼ .02, p ¼ ns, and post-stress cortisol levels, r ¼ .19, p ¼ ns. Additionally, introducing anxiety as a covariate in the main group analyses did not alter the pattern or magnitude of findings.
ARTICLE IN PRESS Cortisol and psychopathic personality traits
Table 1
187
Sample descriptive statistics and group comparisons. Male participants
Age (SD) Anxiety (SD) Levenson Psychopathy Scale Primary psychopathy (SD) Secondary psychopathy (SD)
Female participants
Low psychopathic personality traits (n ¼ 20)
High psychopathic personality traits (n ¼ 21)
Low psychopathic personality traits (n ¼ 21)
High psychopathic personality traits (n ¼ 22)
F
18.52 (1.05) 34.82 (6.79)
18.50 (0.83) 36.00 (9.29)
18.38 (0.80) 37.67 (10.94)
18.50 (1.14) 39.27 (10.58)
.31 .88
23.75a (3.97) 18.35a (2.52)
42.61b (4.51) 24.49b (3.85)
20.76a (2.59) 17.40a (4.56)
39.59b (4.31) 22.60b (5.63)
165.86** 12.80**
(3,80)
X 2ð3;N¼84Þ Ethnicity (% Minority)
55%
a
29%
ab
14%
b
50%
a
9.67*
Note: Means with different subscripts were significantly different (po.05) in pairwise comparisons using the Chi square test for the ethnicity variable and the Tukey’s HSD test for all other variables. *po.05 and **po.001.
groups. Additionally, male and female groups with similar designations (e.g., low or high psychopathic personality traits) did not differ significantly in level of psychopathic personality traits. This removed the possibility that any documented gender differences could be accounted for by differing levels of psychopathic personality traits. Analogous results were found for Levenson Secondary Psychopathy scores (i.e., psychopathic behavioral features). The groups did differ significantly in percentage of minority participants. Males characterized by low psychopathic personality traits and females characterized by high psychopathic personality traits had a significantly greater percentage of minority participants than females low in psychopathic personality traits.4 In order to test the main study hypotheses, a 2*2*2 mixeddesign ANOVA was conducted, with group status (low or high psychopathic personality traits) and gender as betweensubjects variables, and time of saliva sample (pre-stress and post-stress) as a within-subjects variable. Of note, the observed range of pre-stress (M ¼ .27 mg/dL, SD ¼ .14, range ¼ .07–.85) and post-stress cortisol levels (M ¼ .41 mg/dL, SD ¼ .27, range ¼ .10–1.62) were within normal parameters for the demographic characteristics of the sample (e.g., Habra et al., 2003; Kudielka et al., 2004). None of the cortisol values were outside of established parameters within and across the recruited groups. The ANOVA revealed a significant 3-way interaction, F (1,80) ¼ 9.73, po0.05, that qualified any assertions that could be made about main effects. These analyses were also conducted introducing Levenson SRPS Secondary Psychopathy scores as a covariate. This was done to assure that documented group differences were uniquely related to 4
Ethnicity information was presented strictly for descriptive purposes. Although no a priori hypotheses were made concerning ethnicity, minority status displayed non-significant associations to pre-stress, t (82) ¼ 1.41, p ¼ ns, and post-stress cortisol levels, t (82) ¼ 0.04, p ¼ ns. Furthermore, introducing minority status as a covariate in the main group analyses did not alter the pattern or magnitude of findings.
psychopathic personality traits rather than covarying levels of psychopathic behavioral features (i.e., impulsive and antisocial behavior) tapped by the Secondary Psychopathy subscale. A preliminary analysis revealed non-significant bivariate associations between the Secondary Psychopathy subscale and both pre-stress, r ¼ .05, p ¼ ns, and post-stress cortisol levels, r ¼ .14, p ¼ ns. Further, the introduction of this covariate did not alter the pattern or magnitude of the reported findings. Fig. 1 provides a graphical representation of the threeway interaction. While psychopathic personality traits moderated cortisol response to the stress induction, this effect was limited to the male participants. Consistent with prediction, pairwise comparisons confirmed that males low in psychopathic personality traits exhibited a statistically significant increase in cortisol following the stress induction, po.001, that was lacking for the males elevated in psychopathic personality traits, p ¼ .21. Importantly, male recruitment groups did not differ significantly in pre-stress cortisol levels, p ¼ .99. A comparison of the average increase in cortisol following the stress induction (poststress minus pre-stress cortisol) for males low in psychopathic personality traits (M ¼ .35, SD ¼ .30) and high in psychopathic personality traits (M ¼ .10, SD ¼ .13) revealed a large effect size, d ¼ 1.08 (Cohen, 1992). Female recruitment groups did not differ significantly on pre-stress, p ¼ .99, or post-stress cortisol levels, p ¼ .99. Furthermore, both female groups failed to display significant increases in cortisol in response to the stress induction, p values 4.82.
4. Discussion The current study replicates and extends the recent Loney et al. (2006) report that cortisol production is a biological marker for male psychopathic personality traits. Male participants characterized by elevations in psychopathic personality traits failed to display stress induced increases in cortisol that were present for males low in psychopathic personality traits. This was a large effect (d ¼ 1.08) that
ARTICLE IN PRESS 188
M.M. O’Leary et al.
0.9
males
females
0.8
* low psychopathic traits
salivary cortisol (µg/dl)
0.7
high psychopathic traits
0.6 0.5 0.4 0.3 0.2 0.1
pre
post stress induction
pre
post stress induction
Figure 1 Average pre- and post-stress salivary cortisol levels (mg/dL) by group and gender. As predicted, males low in psychopathic personality traits displayed a significant increase in cortisol relative to comparison groups. Females displayed nominal and nonsignificant increases in cortisol across recruitment groups. *Greater than both the male low psychopathic personality traits/pre-stress condition, po.001, and the male high psychopathic personality traits/post-stress condition, po.01.
was only present for the male participants. Female participants failed to display increases in cortisol following the stress induction regardless of the level of psychopathic personality traits. For males, it was interesting that no differences in prestress (or resting) cortisol levels were documented given that Loney et al. (2006) focused exclusively on resting cortisol and found that male psychopathic personality traits were associated with low resting cortisol. Nevertheless, it is important to reiterate that the Loney et al. study sampled cortisol in the early morning and the current study sampled cortisol in the mid-afternoon. Given the diurnal variability of cortisol production (i.e., peaks and less variability in the morning; stabilizes and more variable in the mid-afternoon), differences in resting cortisol effects are not surprising. After all, morning sampling is generally recommended for comparisons of resting cortisol and mid-afternoon assessments are generally recommended for the assessment of stress-induced changes (Kudielka et al., 2004). Regardless, Loney et al. suggested that resting cortisol may also be a less reliable and valid indicator of stress reactivity given the multitude of daily living factors that can impact resting cortisol levels and the failure to directly assess biological reactivity to a threat stimulus. The current study rigorously controlled for daily living variables that were not controlled for in the Loney et al. study (e.g., recent exercise and smoking) and also contained older participants. Future research should continue to assess the reliability of resting cortisol effects across distinct time periods (e.g., morning and mid-afternoon), particularly given that indicators of resting autonomic nervous system activity (e.g., low resting heart rate) have proven to be reliable markers of psychopathic personality traits (Raine, 2002). However, the assessment of stress-induced changes in cortisol is arguably
a more precise measure of stress reactivity that has the benefit of gauging cumulative biological reactivity to a wide variety of threat stimuli. Stress induced changes also provide more rigorous control for individual differences in resting cortisol related to developmental level and related personality and daily living variables. Methodologically, this could make this measure and associated findings more robust to age and setting of participants. Females elevated in psychopathic personality traits responded as expected and similarly to males elevated in psychopathic personality traits. Perhaps the more intriguing finding was the lack of stress-induced increase in cortisol for female participants characterized by low psychopathic personality traits. The failure of the stress induction to elicit increases in cortisol for the female control participants suggests some important methodological and theoretical considerations for future research. First, it is possible that sociocultural influences are operating to shape sensitivity to the stress induction. While prior research with the TSST has generally produced cortisol responses in males and females (Dickerson and Kemeny, 2004), there is evidence that gender is associated with differences in subjective interpretation of stressful events and related psychobiological responsiveness to stress stimuli (e.g., Kudielka and Kirschbaum, 2005; Stroud et al., 2002). Furthermore, some other recent TSST research has suggested that male salivary cortisol response is greater than female salivary cortisol response (e.g., Kudielka and Kirschbaum, 2005), and this mirrors other recent findings suggesting that higher salivary cortisol responses are found in young men after exposure to acute real-life and laboratory psychological stressors (i.e. academic exams, free speech, mental arithmetic) (Stroud et al., 2002; Kajantie and Phillips, 2006). This suggests that future research will need to carefully consider the nature of
ARTICLE IN PRESS Cortisol and psychopathic personality traits threat stimuli used in psychopathy investigations prior to determining if null effects provide robust evidence that cortisol irregularities are not present for female participants. Young women are generally socialized for a relational orientation by authority figures and peers, and this is contrasted with a sociocultural emphasis on instrumentality and physical dominance for young men (Crick and ZahnWaxler, 2003). Interestingly, the TSST contains a performance-based threat that is arguably more sensitive to an instrumental orientation. Future research should integrate stress induction measures that tap a relational orientation, such as peer rejection paradigm, in order to further examine if sociocultural influences may account in part for the documented findings (cf. Stroud et al., 2002). Prior psychopathy research has largely focused on male participants and has therefore generally failed to discuss the impact of gender socialization on the emotional underreactivity implicated in dominant etiological models. Future research could benefit from more detailed biopsychosocial modeling that accounts for the role of gender socialization in the development and expression of psychopathic personality traits. This has implications for future hormone investigations, but it may also prove useful in other related cognitive and behavioral studies. For example, there is now evidence that females and males elevated in psychopathic personality traits display similarly attenuated eye blink startle to distressing pictures such as body mutilations (Sutton et al., 2002). However, there is also evidence that females elevated in psychopathic personality traits lack hypersensitivity to cues for reward (i.e., reward dominance) that is present for males elevated in psychopathic personality traits (Vitale and Newman, 2001). Similar to the current hormone findings, these prior findings could also be explained by gender socialization practices as indices of reward dominance are more sensitive to an instrumental orientation. Related considerations for future research pertain to the assessment of menstrual cycle and the gender of experimenter conducting the stress manipulations. Although the current study followed a protocol consistent with other research examining menstrual cycle phase through self report (e.g., Smeets et al., 2006), this method is less reliable than biological verification of menstrual phase. Future research should consider directly assessing progesterone levels to verify luteal phase assessment. During the luteal phase, mean salivary progesterone increases dramatically with an average concentration of 300 pg/ml (range ¼ 100–500 pg/ml) (White et al., 2002). Any female participants with salivary progesterone levels less than 100 pg/ml could be excluded or treated separately in analyses. Additionally, future research should consider systematically investigating the impact of experimenter gender on study findings. The current study relied exclusively on female experimenters (for males and females), and this may assist in explaining the female findings given that opposite-gender experimenters could increase the impact of the stress induction. The use of opposite-sex experimenters for female participants could further clarify whether experimenter gender accounts in part for the lack of female findings. The current findings must be interpreted in the context of the following limitations. First, the findings were derived on
189 a regionally bound college sample, and the phone call recruitment methodology could have introduced some selfselection biases. Future research should attempt to replicate the study findings in more diverse samples, particularly given that the study of psychopathic personality traits is often conducted in prison settings. Nevertheless, numerous studies have established the reliability and validity of psychopathic personality traits in non-referred and college-aged samples (e.g., Levenson et al., 1995; Lilienfeld and Andrews, 1996; Frick et al., 2003). Furthermore, the use of a non-referred sample removed the potential confound of prison exposure and accumulating antisocial histories present in many prior psychopathy studies. A separate limitation pertains to the extreme groups recruitment approach. The sampling of participants at the upper and lower ends of the distribution of psychopathic traits is commonly done in non-referred psychopathy studies given evidence that psychopathic traits are non-normally distributed and potentially taxonic in nature (Harris et al., 1994; Vasey et al., 2005). Incidentally, the use of this strategy in the current study resulted in SRPS for males/ females in the high psychopathic personality traits groups that were quite comparable to prior prison-based psychopathy research (Brinkley et al., 2001). Extreme groups recruitment is generally recommended for nascent and exploratory research areas such as the current study focus to assist with detecting trends and guiding future studies (Preacher et al., 2005). Nevertheless, as this research area develops, it could be informative to sample at the middle of the distribution to further explore whether psychopathic traits display linear or non-linear associations to cortisol production. Beyond these sampling and recruitment concerns, the current study only sampled cortisol across two time points. This leaves open the possibility that male psychopathic personality traits are associated with greater latency to a cortisol response rather than an absence of a cortisol response. A common methodology for assessing cortisol that has not been used in the study of psychopathic personality traits and aggression is to take repeated saliva samples in 20 min intervals across a 1 1 12 h testing session. This allows for the assessment of changes in cortisol from baseline to peak cortisol response and subsequent recovery (e.g., Dickerson and Kemeny, 2004; Kirschbaum et al., 1993; Kudielka and Kirschbaum, 2005). The integration of this cortisol methodology could allow for detection of group differences in both the initial stress response as well as recovery of the stress response. It would also assist in rulingout the possibility of latency effects (e.g., delayed rather than lack of cortisol response to stressor). Finally, the current study relied exclusively on one measure of emotional reactivity. As mentioned above, future research should expand the nature of the stress stimuli used in cortisol investigations (e.g., performance versus social threat). However, it would also be beneficial to integrate related laboratory and performance-based measures (e.g., electrodermal activity and eye blink startle measures) that ostensibly measure similar emotional reactivity processes. Emotional reactivity subsumes multiple cognitive (e.g., orientation of attention and cognitive appraisal), behavioral (e.g., fight/flight responses), and physiological (e.g., accelerated heart rate and increased
ARTICLE IN PRESS 190 HPA-axis activity) processes that may vary as a function of sociocultural influences. Directly assessing the association between cortisol and related emotional reactivity indices could greatly assist in discerning the specific processes related to male and female psychopathic personality traits. This type of research should also be sensitive to the increasing specificity of brain regions implicated in the development of psychopathic personality traits (King et al., 2006). In summary, the current findings provide increasing support for the hypothesis that cortisol production is a biological marker for male psychopathic personality traits. With continued replication, this type of research has the potential to enhance etiological modeling through greater specificity of putative biological risk variables (i.e., blunted reactivity of the HPA-axis). Furthermore, it suggests a relatively easy and non-invasive method of assessing emotional reactivity that could potentially be used to gauge impairment levels and associated response to psychosocial treatment for males elevated in psychopathic personality traits.
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