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Brain Informatics (2017) 4:231–239 DOI 10.1007/s40708-017-0068-4 The effect of anger expression style on cardiovascular responses to lateralized cognitive stressors . . . David E. Cox Benjamin B. DeVore Patti Kelly Harrison David W. Harrison Received: 10 February 2017 / Accepted: 4 May 2017 / Published online: 15 May 2017 The Author(s) 2017. This article is an open access publication Abstract To determine the effects of self-reported anger Keywords Hostility Anger Cardiovascular response expression style on cerebrally lateralized physiological Brain asymmetry Laterality responses to neuropsychological stressors, changes in systolic blood pressure and heart rate were examined in response to a verbal ﬂuency task and a ﬁgural ﬂuency task among individ- 1 Introduction uals reporting either ‘‘anger in’’ or ‘‘anger out’’ expression styles. Signiﬁcant group by trial interaction effects was found Elements of the multifaceted emotional construct of anger, for systolic blood pressure following administration of verbal such as hostility, have been shown to be associated with ﬂuency [F(1,54) = 5.86, p\ 0.05] and nonverbal ﬂuency increased risk of negative health outcomes such as cardio- stressors [F(1,54) = 13.68, p\ .001]. Similar interactions vascular disease [1–3], cerebrovascular accident , and the were seen for systolic heart rate following administration of metabolic syndrome [5, 6]. Not surprisingly, anger represents verbal ﬂuency [F(1,54) = 5.86, p\ .005] and nonverbal one of the most frequently investigated emotional constructs ﬂuency stressors [F(1,54) = 13.68, p\ .001]. The corre- over the past decade . Despite the frequency of investiga- sponding results are discussed in terms of functional cerebral tion and the health implications ascribed to anger, the mech- systems and potential implications for physiological models anisms by which this emotional construct impacts of anger. Given the association between anger and negative physiological functions are not fully understood. One mech- physical health outcomes, there is a clear need to better anistic model offered considers speciﬁcally how an individual understand the physiological components of anger. The deals with the experience of anger. This model postulates results of this experiment indicate that a repressive ‘‘anger in’’ individuals may process anger through either externalizing or expression style is associated with deregulation of the right internalizing the feelings. Although there has been substantial frontal region. This same region has been shown to be inti- debate regarding which of these strategies may lead to nega- mately involved in cardiovascular recovery, glucose meta- tive health outcomes, there have been surprisingly few bolism, and blood pressure regulation. empirical investigations examining the strategies underlying these two expression styles. The present research examines changes in functional cerebral systems associated with rele- D. E. Cox vant physiological processes among individuals reporting Florida Gulf Coast University, 10501, FGCU Blvd S., Fort Myers, FL 33965, USA different anger expression styles. B. B. DeVore P. K. Harrison Virginia Polytechnic Institute and State University, Blacksburg, 1.1 Deﬁning anger and anger expression VA 24061, USA D. W. Harrison (&) Before any investigation can be conducted in the area of Department of Psychology, Behavioral Neuroscience anger, the construct must be clearly deﬁned. Many differ- Laboratory, Williams Hall, Virginia Tech, Blacksburg, ent deﬁnitions have been offered, and the construct has VA 24061-0436, USA been divided into multiple constructs and factors. For the e-mail: firstname.lastname@example.org 123 232 D. E. Cox et al. purposes of the current research, anger was operationally 1.2 Physiological sequela of anger deﬁned as a multidimensional construct with distinct affective, behavioral, and cognitive dimensions that There have been numerous investigations into the effects of include speciﬁc physiological elements, which contribute anger on physiological function (for review, see ; see also ). The bulk of the literature in this area concep- to both the experience and expression of the emotion . The affective dimension of anger refers to the emotional tualizes anger as an emotion-induced physiological stres- sor, with the same physiological outcomes associated with state, which occurs in response to an immediate stressor and may vary in both intensity and duration . The environmental stressors . The physiological response to anger is consistent with Selye’s  stress model, which cognitive dimension of anger, also referred to as hostility in the literature, has most frequently been deﬁned as a cog- maintains that the body increases autonomic arousal in nitive phenomenon of an attitudinal nature that subserves response to a stressor. This increase in autonomic arousal the emotional process, but is not an emotion per se . may result in increased cardiovascular activity, glucose The behavioral dimension of anger is simply the behavioral metabolism, and changes in patterns of cortical arousal response to the subjective experience of anger  and [16, 17]. The bulk of this research has been conducted may be expressed outwardly or inwardly . utilizing either cognitive anger (hostility) or affective anger (experience) as the variable of interest (for review, see Anger expression styles refer to the manner in which an individual expresses her/his emotional experience of anger. ). Therefore, it is reasonable to suggest that chronic feelings of anger or the subjective experience of anger are Spielberger et al. (; see also [12, 13]) suggested that the tendency to express one’s anger in an outwardly negative associated with increased autonomic arousal. manner represented an outward-directed style known as In terms of anger expression, there have been fewer anger out (A.O.). Anger out may involve the use of investigations into the physiological responses to both A.O. aggressive actions (e.g., assaultive behavior, destruction of and A.I. expression styles. However, there has been some property, or making offensive gestures) and/or aggressive evidence that A.I., as measured by the Anger-In Scale of verbal behavior (e.g., insults, offensive/inappropriate lan- the State-Trait Anger Expression Inventory (STAXI; ), guage, or shouting). Individuals displaying the A.O. style is associated with increased incidence of coronary artery may choose targets for hostile or aggressive behavior if the disease , increased blood pressure in response to anger provocation , and poorer response to therapeutic target is seen as even remotely related to the cause of their anger, including mere proximity when the outburst occurs interventions . Findings such as these suggest that there may be different patterns of physiological responses to . Conversely, the concept of anger in (A.I.) refers to the extent to which individuals suppress anger when they are anger based on expression style. experiencing this negative emotion . High levels of anger suppression have been found to lead to the angry 1.3 Functional systems theory feelings being suppressed and replaced with guilt, anxiety and depression as the person blames himself for the The key to the neuropsychological investigation of emo- problems surrounding the anger-provoking situation . tional expression lies in Luria’s  functional cerebral Interaction among the dimensions of anger and anger systems theory and Kinsbourne’s  cerebral space the- expression style is of particular interest in the current ory. The functional cerebral systems model proposes that there are speciﬁc coordinated regions of the brain that are research. According to Spielberger and colleagues , individuals with a higher degree of trait-like cognitive utilized to complete certain tasks. The functional systems model proposes that multiple regions in different parts of anger are more likely to have more frequent state-like experiences of affective anger. Once an individual expe- the brain may be involved in similar tasks, so while there riences affective anger, the emotion may be expressed may be evidence of diffuse activation in a given process outwardly or repressed. Although any individual who (e.g., expressive speech), the activation patterns will be experiences anger may employ an anger expression style, consistent for that particular activity across individuals individuals with chronic, state-like anger are more likely to . The idea of functional cerebral space maintains that perceive events in a negative manner and experience anger tasks (cognitive, motor, or emotional) require utilization of cerebral resources within a given functional system. If the more frequently . Therefore, these individuals will demonstrate persistent and consistent patterns of anger functional systems that underlie completion of each of two tasks are close in proximity, decrements in performing one repression or expression and thus be vulnerable to any effects caused by the expression style. For this reason, the of the tasks will be especially evident [23, 25, 26]. The functional cerebral systems approach has been uti- current research is particularly interested in the effects of the differing expression styles among those individuals lized in a number of investigations on the effect of hostility with high levels of trait-like cognitive anger. and anger on cardiovascular functions. Research in the area 123 The effect of anger expression style on cardiovascular responses to lateralized cognitive… 233 of cardiovascular responses to cognitive and emotional demonstrate increased systolic blood pressure and heart stressors has demonstrated some lateralizing results. rate in response to a nonverbal ﬂuency task, individuals Demaree and Harrison  predicted increased sympa- reporting a repressive A.I. style would show signiﬁcantly thetic arousal (increased systolic blood pressure, diastolic greater increases compared to those reporting an expressive blood pressure, and heart rate) following cold-pressor A.O. style. Conversely, we predicted that individuals exposure at the left arm. Results supported this prediction, reporting an expressive A.O. style would show increases in with both low- and high-hostile males evidencing increases systolic blood pressure and heart rate in response to a in systolic blood pressure, diastolic blood pressure, and verbal ﬂuency task, while individuals reporting a repressive heart rate. Moreover, the high-hostile group was shown to A.I. style would show decreased heart rate and blood be signiﬁcantly more reactive to the cold-pressor as evi- pressure in response to a verbal ﬂuency measure. denced by a signiﬁcant group by condition interaction for the heart rate data. Thus, signiﬁcant global sympathetic arousal was not found for the high-hostile group, but evi- 2 Methods dence of increased sympathetic tone was noted. Rhodes and Harrison  presented a similar ﬁnding of a signiﬁ- 2.1 Participants cant interaction between group (low- and high-hostile) and exposure to cold-pressor stress at the left arm. Results Participants were recruited from the undergraduate psy- showed increased cardiovascular reactivity (heart rate) in chology population. They completed an online pre- the high-hostile group in response to the stressor. Low- screening that included an Informed Consent Form; a hostiles displayed decreased heart rate following the cold- Medical History Questionnaire; the Coren, Porac, and pressor, whereas high-hostiles displayed increased heart Duncan Laterality Questionnaire ; the Cook-Medley rate following the stressor. Hostility Scale ; and the State-Trait Anger Expression Exploration of hemispheric control of sympathetic Inventory . In order to control for potential laterality response, particularly as it relates to blood pressure and confounds and overall cognitive deﬁcits associated with overall heart rate regulation, indicates general control of substance or structural inﬂuence, participants reporting sympathetic response by the right hemisphere, with left-hand dominance, a history of brain-related insult (e.g., parasympathetic control lateralized to the left hemisphere stroke, seizure, and traumatic brain injury.), use of psy- . Taking into account, right hemispheric dominance for chotropic medications or signiﬁcant physical or mental sympathetic response is an important component when health difﬁculties that would prohibit or limit their partic- looking at the potential for differing anger expression ipation were excluded. Additionally, to ensure appropriate levels of trait-like cognitive anger, participants had to score styles. If, as theorized, taxation of right frontal lobe resources allows for an unbridling of posteriorly located 29 or above on the Cook-Medley Hostility Scale. To ensure neural regions, it is presumed that tasks which are directed appropriate expression of the different anger styles, clinical toward the right hemisphere would result in greater acti- norms for the State-Trait Anger Expression Inventory vation of the sympathetic response. Similarly, if anger ([70th percentile) were used as cutoffs for inclusion in the suppression via right frontal lobe control exhausts right experiment. Participants who had been included in other frontal lobe resources, consequent release of sympathetic studies within the laboratory and had already been shown control is expected to result in increased variability within to be in the high-hostile range were referred to the online heart rate and blood pressure. screening. Individuals participating in this initial screening Considering the various health and psychological were awarded one course credit point for their impacts associated with anger expression, the current participation. research investigated the effects of self-reported anger Of the 377 students completing the online screening, 62 expression style on cerebrally lateralized physiological met criteria for inclusion in the experimental phase and responses to a neuropsychological stressor. Speciﬁcally, were scheduled for follow-up testing. Among those not this research examined changes in systole and grip strength included in the experimental phase, most were excluded for in response to a verbal ﬂuency task and a ﬁgural ﬂuency not meeting scoring criteria on the Cook-Medley Hostility task. Previous research has demonstrated that the verbal Scale (n = 256) or the State-Trait Anger Expression ﬂuency and ﬁgural ﬂuency tasks are appropriate for elic- Inventory (n = 97) with others (n = 5) excluded for iting performance-related lateralized activation , as medical or psychiatric conditions (n = 5). As the experi- verbal ﬂuency has been shown to be a stressor for the left ment advertisement indicated that right-handed men were anterior region, and design ﬂuency has the same effect on being recruited, few individuals were excluded on the basis the right anterior region [29, 30]. Based on the preceding of handedness (n = 3) or gender (n = 2). To ensure test– review, we predicted that although both groups would retest reliability, initially accepted participants were 123 234 D. E. Cox et al. administered the screening measures a second time in the 3.3 Blood pressure and heart rate laboratory. Further exclusion criteria included participants who scored differently on the screening measures at the The Norelco Healthcare Electronic Digital Blood Pressure/ second administration. Speciﬁcally, individuals who scored Pulse Meter (Model HC3030; Norelco Health Group, Inc; New York) was used to provide an oscillometric measure in the upper one-third of scores on the CMHI during the online screening, but then scored signiﬁcantly lower at the of systolic blood pressure and heart rate. This instrument has been shown to demonstrate adequate accuracy and follow-up assessment (n = 9). Finally, a small set of individuals reporting a primarily A.I. expression style reliability in empirical comparison trials . (n = 5) were randomly excluded to ensure equal anger expression group sizes. The ﬁnal analysis included 56 high- 3.4 Procedure hostile men between the ages of 18 and 24 years (M = 19.50, SD = 1.50). Subjects meeting full criteria on the online screen were contacted to participate in the experimental phase, and an appointment was made at that time. Upon arrival, each 3 Materials participant completed an Informed Consent Form. Subjects then completed the Medical History Questionnaire, 3.1 Questionnaires CPDLT, CMHI, and STAXI. Consistent with previous research from this laboratory, only subjects scoring in the General medical and psychiatric health was assessed using highest one-third of scores on the CMHI were considered a brief inventory designed for use in neuropsychological to be experiencing high levels of cognitive anger research [1, 32]. The Coren–Porac–Duncan Laterality Test [11, 27, 37, 38]. Scores over 29 on the CMHI were among  was utilized to determine laterality. Cognitive anger the upper one-third of scores obtained by all participants in was assessed using the Cook-Medley Hostility Inventory the online screening. Therefore, only those subjects with (CMHI; ), which consists of 50 dichotomous ‘‘true/- CMHI scores of 29 or higher were retained for the remainder of the experiment. false’’ items broken into six categories (hostile attributions, cynicism, hostile affect, aggressive responding, social In order to compare anger expression styles, subjects were placed in groups based on STAXI scores on the anger in scale avoidance, and other). The State-Trait Anger Expression Inventory (STAXI; ) is a 57-item, 4-point scale (AIS) and anger out scale (AOS). Cutoff scores for group inclusion were determined using clinical norms on the inventory, consisting of subscales that measure anger intensity and overall angry feelings. The STAXI has been expression scales (AIS [ 70th percentile = anger in; AOS [ 70th percentile = anger out). Since some subjects normed for individuals 16–63 years of age and takes approximately 5–10 min to administer. Elevated T scores did not cleanly ﬁt into an expression category, due to both have been associated with speciﬁc anger expression styles. scales being elevated above the 70th percentile, individuals It was used to assess anger expression style since it is were grouped according to their highest elevation. For purported to measure transient (state) anger expression example, a subject scoring on the 73rd percentile on the (anger out) and anger inhibition (anger in). anger in scale and the 95th percentile on the anger out scale would be placed in the anger out group. Assessment of anger expression style at the follow-up assessment revealed an 3.2 Neuropsychological measures unequal distribution of participants scoring higher on the A.I. (n = 33) and A.O. (n = 28) scales. A total of 17 participants The Controlled Oral Word Association Test (COWAT ) functions as a measure of verbal ﬂuency by asking partici- demonstrated clinically signiﬁcant elevations on both pants to spontaneously name words beginning with an expression scales and were distributed between the A.I. identiﬁed speciﬁc letter (‘‘F’’ for example) and takes (n = 12) and A.O. (n = 5) groups. As mentioned in the approximately 5–10 min to administer. This instrument has exclusion criteria, in order to ensure an equal distribution of been demonstrated to differentially stress left cerebral sys- individuals in each expression style group, a portion of tems or circuits processing logical linguistic or propositional participants who exhibited elevations on the A.I. scale were speech . The Ruff Figural Fluency Test (RFFT)  not retained for the experimental phase (n = 5). Final consists of ﬁve separate parts and takes approximately 5 min grouping resulted in an equal distribution of participants in both A.I. (n = 28) and A.O. (n = 28) groups, with a roughly to administer. It has been shown to provide information regarding nonverbal capacity for ﬂuid and divergent think- equivalent distribution of individuals demonstrating signif- icant elevations for either A.I. (n = 7) or A.O. (n = 5). ing. This instrument has been further demonstrated to dif- ferentially stress right cerebral systems or circuits processing Baseline systolic blood pressure and heart rate data were ﬁgural ﬂuency or design drawing . collected from participants in accordance with previous 123 The effect of anger expression style on cardiovascular responses to lateralized cognitive… 235 procedures used in this laboratory [27, 30, 36], with two versus an overall sample trend. However, to maintain the readings taken. A third reading was taken if the initial two sample size and integrity of the overall data results, these readings were more than 10 mmHg (for systolic blood scores were included in the statistical analysis. Bonferroni pressure) or beats per minute (for heart rate) apart. Fol- correction was used to correct for multiple comparisons. lowing the baseline physiological measurements, partici- pants completed measures of either verbal or ﬁgural 4.1 Systole ﬂuency (Controlled Oral Word Association Test, COWAT ; Ruff Figural Fluency Test, RFFT ). Immediately Consistent with the stated hypotheses, systolic blood following completion of the ﬂuency measure, participants’ pressure varied signiﬁcantly as a function of anger blood pressure and heart rate were taken as measures of expression style (Figs. 1, 2). Mean systolic blood pressure, physiological reactivity to the task. Following the ﬁrst diastolic blood pressure, and heart rate values after com- neuropsychological measure, participants completed the pletion of the COWAT and RFFT are presented in Table 2. converse measure. Following completion of the second An ANOVA was used to examine the effects of verbal ﬂuency test, blood pressure and heart rate data were ﬂuency (COWAT performance) on systolic blood pressure. obtained utilizing the method described above. Participants No signiﬁcant main effect of trial [F(1,54) = .94, p = .34] were given a 3-min rest period between the completion of Estimated Marginal Means of cowasys the ﬁrst task and the start of the second task. Neuropsy- STAXIrate chological test administration was counterbalanced to Anger-In control for any possible order effects. Anger-Out 4 Results Systolic blood pressure Anger expression groups did not differ in terms of laterality (mmHg) preferences (CPDLT; t = 1.53, 53, p = .879), reported tobacco smoking (Fagerstrom; t =-.537, 54, p = .593), CMHI scores (t = .769, 53, p = .445), baseline systolic blood pressure (t = .177, 54, p = .860), diastolic blood pressure (t = 1.122, 54, p = .267), and heart rate (t = .634, 53, p = .529). Mean values for baseline measures are pre- sented in Table 1. An ANOVA was used for each trial, Pre COWAT Post COWAT consisting of pre-task and post-task, comparing systole and Trial heart rate consecutively, by anger expression style. Of note, Fig. 1 COWAT systolic blood pressure, group by time interaction some of the statistical power seen in the results may be from signiﬁcant elevations in individual AI/AO scale scores Estimated Marginal Means of rfftsys STAXIrate Table 1 Baseline means and SD for CPDLT, fagerstrom, CMHI, Anger-In systole, diastole, and heart rate Anger-Out Anger expression style N Mean SD CPDLT In 28 9.39 1.59 Systolic blood Out 28 9.32 1.88 pressure Fagerstrom In 28 .25 .52 (mmHg) Out 28 .32 .48 CMHI In 28 34.46 2.80 Out 28 33.93 2.40 Systole In 28 128.36 6.69 Out 28 128.04 6.87 Diastole In 28 70.00 3.78 Out 28 68.79 4.30 Pre RFFT Post RFFT Trial Heart rate In 28 73.57 2.73 Out 28 73.11 2.75 Fig. 2 RFFT systolic blood pressure, group by time interaction 123 236 D. E. Cox et al. Table 2 Means and SD for Anger expression style N Mean Standard deviation post-ﬂuency systole, diastole, and heart rate COWAT systole In 28 126.89 7.55 Out 28 130.71 7.48 COWAT diastole In 28 70.11 3.66 Out 28 68.93 4.04 COWAT HR In 28 72.61 4.19 Out 28 73.39 3.20 RFFT systole In 28 133.57 7.05 Out 28 126.54 6.79 RFFT diastole In 28 70.18 3.57 Out 28 69.25 4.17 RFFT HR In 28 73.29 4.19 Out 28 72.79 3.20 or anger expression style [F(91,54) = .937, p = .34] was Estimated Marginal Means of cowahr found. However, there was a signiﬁcant interaction of trial 73.6 STAXIrate and anger expression style [F(1,54) = 10.89, p = .02]. Anger-In Anger-Out The Cohen’s effect size value for the interaction (d = .508) 73.4 indicated a moderate practical signiﬁcance. Multiple comparisons of the interaction effects showed that partic- ipants in the A.O. expression style group demonstrated 73.2 signiﬁcantly higher systolic blood pressure following the Beats Per completion of a verbal ﬂuency measure [t(27) =-2.718, Minute p = .-011]. However, our hypothesis that individuals in the A.O. group would demonstrate a signiﬁcant decrease in systolic blood pressure following completion of the 72.8 COWAT was not supported [t(27) = 1.88, p = .07]. Par- ticipants in the A.I. group did not show a signiﬁcant 72.6 decrease in systolic blood pressure after completing the verbal ﬂuency measure. Pre COWAT Post COWAT Trial In terms of the effects of a nonverbal ﬂuency (RFFT performance) measure on systolic blood pressure, main Fig. 3 COWAT heart rate, group by time interaction effects were found for trial [F(1,54) = 16.67, p = .000] and anger expression style [F(1,54) = 4.30, p = .04], both (Figs. 3, 4). No signiﬁcant main effect was found for trial in the hypothesized direction. Additionally, a signiﬁcant [F(1,54) = 1.74, p = .193] or anger expression style trial by anger expression style interaction effect was found [F(1,54) = .048, p = .83]. Conversely, there was a signiﬁ- [F(1,54) = 54.47, p = .000]. The Cohen’s effect size for cant trial by anger expression style interaction effect this interaction (d = 1.01) was high, suggesting that the [F(1,54) = 5.89, p = .02]. However, this interaction had a observed difference was slightly greater than one standard low Cohen’s effect size value (d = .229). Multiple com- deviation. Multiple comparisons of the interaction effect parisons of this interaction indicated that participants in the showed that participants in the anger in group demon- anger in expression style group demonstrated non-signiﬁcant strated signiﬁcant increases in systolic blood pressure reductions in heart rate [t(27) = 1.09, p = .28]. Conversely, [t(27) = 6.92, p = .000], and individuals in the anger out participants in the anger out group demonstrated a non-sig- group demonstrated signiﬁcant decreases in systolic blood niﬁcant increase in heart rate following the completion of a pressure [t(27) = 4.10, p = .000]. verbal ﬂuency measure [t(27) = 2.71, p = .03]. In terms of the effects of a nonverbal ﬂuency measure on 4.2 Heart rate heart rate, main effects were found for trial [F(1,54) = 13.29, p = .001] and anger expression style [F(1,54) = As predicted in the hypotheses, these results demonstrated 7.34, p = .009]. Again, these results were in the expected signiﬁcant changes in heart rate in response to completion of direction. Additionally, a signiﬁcant trial by anger verbal ﬂuency measure based on anger expression style expression style interaction effect was found [F(1,54) = 123 The effect of anger expression style on cardiovascular responses to lateralized cognitive… 237 Estimated Marginal Means of rffthr experiment. Among individuals reporting an expressive A.O. style, the model predicts greater utilization of left STAXIrate frontal resources, which is consistent with behavioral Anger-In Anger-Out activation . The addition of a verbal ﬂuency stressor would provide further competition for left frontal resour- ces, causing signiﬁcant activation of the left frontal area. The concept of balance in the quadrant model predicts that Beats signiﬁcant activation of the left frontal region may lead to Per compensating deactivation of the right frontal region. As Minute cardiac control has been linked to the right frontal region (, see also ), deactivation of the region would be expected to result in deregulation of cardiovascular responses. Conversely, among individuals reporting a repressive A.I. style, the left frontal activation produced by verbal ﬂuency tasks is not competing for resources with the Pre RFFT Post RFFT individuals’ anger expression style. Therefore, the frontal Trial regions are balanced and the available right frontal resources allow for greater capacity to attend to cardio- Fig. 4 RFFT heart rate, group by time interaction vascular regulation, resulting in a decrease in systolic blood 57.12, p = .000]. The Cohen’s effect size value for this pressure and heart rate. interaction (d = 1.27) was also high. Multiple comparisons Similarly, the cardiovascular responses to the nonverbal of the interaction effect showed that participants in the ﬂuency measure among individuals reporting a repressive anger in group demonstrated signiﬁcant increases in heart A.I. expression style are supportive of the quadrant model rate [t(27) =-7.33, p = .000]. Conversely, individuals in and the anger expression model proposed here. The anger the anger out group demonstrated signiﬁcant decreases in expression model predicts greater utilization of right frontal systolic blood pressure [t(27) = 3.03, p = .005]. resources (consistent with behavioral inhibition) for the repressive A.I. anger expression style. The additional stres- sor of a nonverbal ﬂuency measure would provide compe- 5 Discussion tition for these frontal resources, resulting in increased right frontal activation. This right frontal activation is in direct Hypotheses related to cardiovascular responses to lateral- competition for the right frontal resources, which have been ized neuropsychological stressors were generally supported demonstrated to be responsible for inhibition of right parietal by the current experiment. Signiﬁcant interactions between and temporal regions. Increased activation of these tem- anger expression styles and cardiovascular responses were poroparietal regions have been proposed to be responsible found for both verbal and nonverbal ﬂuency stressors. for increases in sympathetic tone . Therefore, signiﬁcant Participants reporting an expressive ‘‘anger out’’ (A.O) increases in systolic blood pressure and heart rate in this style demonstrated signiﬁcant systolic blood pressure condition are congruent with the predictions of the model. increases and a non-signiﬁcant increase in heart rate fol- The results regarding cardiovascular responses to the lowing administration of a verbal ﬂuency measure, while nonverbal ﬂuency measure among participants reporting an participants reporting a repressive ‘‘anger in’’ (A.I) style expressive A.O. style are not readily interpreted under the demonstrated non-signiﬁcant decrease in these cardiovas- framework of the quadrant model. One possible explana- cular responses. Conversely, participants reporting a tion for these results, congruent with the quadrant model, repressive A.I. expression style demonstrated signiﬁcant involves the element of balance. It may be that individuals increases in systolic blood pressure and heart rate follow- with an expressive A.O. style have a greater capacity for ing a measure of nonverbal ﬂuency, while participants design ﬂuency tasks and therefore do not process this task reporting an A.O. expression style demonstrated signiﬁcant as a cognitive stressor. Although there may be competition decreases in systolic blood pressure and heart rate to the for right frontal resources by the design ﬂuency task and same neurocognitive stressor. cardiovascular control, the left frontal region is not acti- These results are best explained under the framework of vated (as the task is not stressful to this group, there is no the quadrant model that, in conjunction with the theories of activation of this region) and can balance the heightened functional cerebral systems and cerebral space, forms the activity of the right frontal region, allowing for greater foundation for the anger expression model employed in this control of cardiovascular functions. 123 238 D. E. Cox et al. Overall, the current experiment was supportive of the expression style is associated with deregulation of the right proposed anger expression theory within the larger context frontal region. This same region has been shown to be of the quadrant model. As suggested in the preceding lit- intimately involved in cardiovascular recovery, glucose erature review, the elements of competition and balance metabolism, and blood pressure regulation. account for the bulk of the ﬁndings reported here. Direct Compliance with ethical standards competition for right frontal resources such as nonverbal ﬂuency, muscular control of the left extremities, and reg- Conﬂict of interest On behalf of all authors, the corresponding ulation of systolic blood pressure demonstrated signiﬁcant author states that there is no conﬂict of interest. deregulation among participants reporting a repressive A.I. expression style. Direct competition may also be shown to Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://crea cause individuals reporting an expressive A.O. style tivecommons.org/licenses/by/4.0/), which permits unrestricted use, reduced efﬁciency in verbal ﬂuency, as measured by per- distribution, and reproduction in any medium, provided you give severative errors. These results further suggest that hemi- appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were spheric balance, as deﬁned in the quadrant model, can be made. shown to cause deregulation of cardiovascular control and left-hand grip strength among individuals reporting an expressive A.O. style. References The current experiment was not without limitations. Future research in this area should be conducted utilizing a 1. 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Everson SA, Kaplan GA, Goldberg DE, Lakka TA, Sivenius J, order to fully investigate the role that anger expression Salonen JT (1997) Anger expression and incident stroke style may play in the ﬁndings of cerebral lateralization prospective evidence from the Kuopio Ischemic Heart Disease studies (e.g., [42, 43]), future experiments should be Study. Stroke 30:523–528 5. Walters RP, Harrison PK, DeVore BB, Harrison DW (2016) designed to examine these differences across levels of Capacity theory: a neuropsychological perspective on shared cognitive anger. neural systems regulating hostile violence prone behavior and the Another limitation for consideration is the usage of the metabolic syndrome. J Neurol Disord Epilepsy 3(1):1014–1030 identiﬁed neuropsychological instruments as indices of 6. Walters RP, Harrison PK, Campbell RW, Harrison DW (2016) hemispheric activation. While the constructs used in the Frontal lobe regulation of blood glucose levels: support for the limited capacity model in hostile violence-prone men. Brain experiment are widely accepted as generally implicating Inform 3(4):221–231 left versus right activity, neither the RFFT nor the COWAT 7. Eckhardt CI, Deffenbacher J (1995) Diagnosis of anger disorders. can be said to exclusively activate a given hemisphere. In: Kassinove H (ed) Anger disorders: deﬁnition, diagnosis and Finally, future investigations of anger need to provide treatment. Taylor & Francis, Washington, DC 8. Spielberger CD (1988) Manual for the state-trait anger expression greater focus into the role of the posterior cerebral systems. inventory (STAXI). Psychological Assessment Resources, Odessa Although the results of this experiment demonstrate a clear 9. Spielberger CD, Reheiser EC, Syderman SJ (1995) Measuring the relationship between frontal regions and anger expression experience, expression, and control of anger. Issues Compr Pediatr Nurs 18:207–232 styles, the potential contributions of posterior cerebral 10. Smith TW (1994) Concepts and methods in the study of anger, systems are not addressed. In particular, the potential role hostility, and health. In: Siegman AW, Smith TW (eds) Anger, and neuroanatomical underpinnings of the right posterior hostility and the heart. Earlbaum, Hillsdale region in relation to perception of anger and the left pos- 11. Weiner B (1995) Inferences of responsibility and social motiva- tion. In: Zanna MP (ed) Advances in experimental social psy- terior region in relation to cognitive appraisals, and how chology. Academic Press, San Diego these systems may be related to anger expression, warrant 12. Harmon-Jones E, Harmon-Jones C (2015) Neural foundations of further investigation. motivational orientations. Handbook of biobehavioral approaches Given the association between anger and negative to self-regulation. Springer, New York, pp 175–187 13. Harrison DW (2015) Brain asymmetry and neural systems: physical health outcomes (e.g., cardiovascular disease, foundations in clinical neuroscience and neuropsychology. increased risk of cerebrovascular accident, metabolic syn- Springer International, Cham drome, and hypertension), there is a clear need to better 14. Spielberger CD, Ritterband LM, Sydeman SJ, Reheiser EC, understand the physiological components of this emotion. Unger KK (1995) Assessment of emotional states and personality The results of this experiment indicate that a repressive A.I. traits: measuring psychological vital things. In: Butcher NJ (ed) 123 The effect of anger expression style on cardiovascular responses to lateralized cognitive… 239 Clinical personality assessment: practical approaches. Oxford 37. Demaree HA, Higgins DA, Williamson JB, Harrison DW (2002) University Press, New York Asymmetry in hand grip strength and fatigue in low- and high- 15. Selye H (1976) Stress in health and disease. Butterworth, Reading hostile men. Int J Neurosci 112:415–428 16. Andreassi JL (1989) Psychophysiology: human behavior and 38. Harrison DW, Gorelczenko PM (1990) Functional asymmetry for physiological responses. Lawrence Erlbaum Associates, Hillsdale facial affect perception in high- and low-hostile men and women. 17. Morruzzi G, Magoun H (1949) Brain stem reticular formation Int J Neurosci 55:89–97 and activation of the EEG. Electroencephalogr Clin Neurophysiol 39. Benton AL, Hamsher KS, Sivan AB (1978) Multilingual aphasia 1:455–473 examination, 3rd edn. AJA Associates Inc, Iowa City 18. Cox DE, Harrison DW (2008) Models of anger: contributions 40. Wittling W (1995) Brain asymmetry in the control of autonomic- from psychophysiology, neuropsychology and the cognitive physiologic activity. In: Davidson RJ, Hugdahl K (eds) Brain behavioral perspective. Brain Struct Funct 5:1171–1187 asymmetry. The MIT Press, Cambridge 19. Spielberger CD, Johnson EH, Russell SF, Crane RS, Jacobs G, 41. Holland AK, Newton SE, Hinson DW, Hardin J, Coe M, Harrison Worden TJ (1983) Assessment of anger: the state-trait scale. In: DW (2014) Physiological and behavioral indices of hostility: an Butcher JN, Spielberger CD (eds) Advances in Personality extension of the capacity model to include exposure to affective assessment, vol 2. Earlbaum, Hillsdale stress and right lateralized motor stress. Laterality Asymmetries 20. Yousﬁ S, Matthews G, Amelang M, Schmidt-Rathjens C (2004) Body Brain Cogn 19(5):560–584 Personality and disease: correlations of multiple trait scores with 42. Davidson RJ (1998) Affective style and affective disorders: per- various illnesses. J Health Psychol 9:627–647 spectives from affective neuroscience. Cogn Emot 12:307–330 21. Del Vecchio T, O’Leary SG (2006) Antecedents of toddler 43. Harmon-Jones E, Sigelman JHD, Bohlig A, Harmon-Jones C aggression: dysfunctional parenting in mother–toddler dyads. (2003) Anger, coping, and frontal cortical activity: the effect of J Clin Child Adolesc Psychol 35:194–202 coping potential on anger-induced left frontal activity. Cogn 22. Erwin BA, Heimberg RG, Schreier FR, Liebowitz MR (2003) Emot 17:1–24 Anger experience and expression in social anxiety disorder: pretreatment proﬁle and predictors of attrition and response to David E. Cox is a Clinical Neuropsychologist and Assistant Professor cognitive behavioral treatment. Behav Ther 34:331–350 at Florida Gulf Coast University. He earned his doctoral degree in 23. Kinsbourne M (1978) Asymmetrical function of the brain. clinical neuroscience and neuropsychology at Virginia Polytechnic Cambridge University Press, Oxford Institute under the supervision of David W. Harrison, Ph.D. and 24. Luria AR (1973) The frontal lobes and the regulation of behavior. completed his postdoctoral fellowship at the University of Florida In: Pribram KH, Luria AR (eds) Psychophysiology of the frontal under the supervision of Kenneth Heilman, M.D., Ph.D. lobes. Academic Press, Oxford 25. Comer CS, Harrison PK, Harrison DW (2015) The dynamic opponent relativity model: an integration and extension of Benjamin B. DeVore is working on his PhD in clinical neuropsy- capacity theory and existing theoretical perspectives on the chology at Virginia Tech University. His research focuses on the neuropsychology of arousal and emotion. SpringerPlus 4(1):1–21 neural impacts of emotional trauma and the resulting physiological/ 26. Klineburger PC, Harrison DW (2015) The dynamic functional behavioral changes associated with emotional trauma. Brad is a capacity theory: a neuropsychological model of intense emotions. reservist with the U.S. Navy who will complete his internship with the Cogent Psycho 2(1):1029691 Navy to work with service members recovering from PTSD. He 27. Demaree HA, Harrison DW (1997) Physiological and neuropsy- received his M.S. from Lipscomb University in Nashville, TN, and his chological correlates of hostility. Neuropsychologia 35:1405–1411 B.S. from U.C. Santa Barbara. 28. Rhodes RD, Harrison DW, Demaree HA (2002) Hostitlity as a moderator of physiological reactivity and recovery to stress. Int J Patti Kelly Harrison is currently a lecturer in the psychology Neurosci 112:167–186 department at Virginia Tech. She received her B.S. in psychology and 29. Foster PS, Williamson JB, Harrison DW (2005) The Ruff Figural French from Washington College and her M.S. and Ph. D. from the Fluency Test: heightened right frontal lobe delta activity as a University of Georgia. She is currently the director for undergraduate function of performance. Arch Clin Neuropsychol 20:427–434 research of the Behavioral Neuroscience Laboratory at Virginia Tech. 30. Williamson JB, Harrison DW (2003) Functional cerebral asym- She is interested in sex differences in laterality and emotion. metry in hostility: a dual task approach with ﬂuency and car- diovascular regulation. Brain Cogn 52:167–174 David W. Harrison received his doctoral degree from the University 31. Coren SP, Porac C, Duncan P (1979) A behaviorally validated of Georgia. Upon completion of his post-doctoral fellowship and self-report inventory to assess four types of lateral preferences. faculty appointment at Georgia, he accepted an appointment as the J Clin Neuropsychol 1:55–64 Director of the Behavioral Neuroscience Laboratory at Virginia 32. Cook W, Medley D (1954) Propose hostility and pharisaic-virtue Polytechnic Institute. He has published extensively with theoretical scales for the MMPI. J Appl Psychol 38:414–418 developments in the areas of clinical, behavioral, cognitive, and 33. Spreen O, Benton AL (1977) Neurosensory centre for the com- affective neuroscience. His recent book, entitled Brain Asymmetry & prehensive examination of aphasia (NCCEA). University of Neural Systems: Foundations in Clinical Neuroscience and Neu- Victoria Neuropsychological Laboratory, Australia ropsychology was on the Springer International Publishing Company 34. Lezak MD, Howieson DB, Bigler ED, Tranel D (2012) Neu- (Biomedical Neuroscience) ‘‘best seller list’’ (top 25 percent) in 2016 ropsychological assessment, 5th edn. Oxford University Press, with some 30,000 downloads by 2017. This was Springer’s ‘‘Featured New York Book in Biomedical Neuroscience,’’ for the Society for Neuroscience 35. Ruff RM, Light RH, Evans RW (1987) The Ruff Figural Fluency (SFN, 2015). Test: a normative study with adults. Dev Neuropsychol 3:37–51 36. Harrison DW, Kelly PL (1987) Home health care: accuracy, calibration, exhaust, and failure rate comparisons of digital blood pressure monitors. Med Instrum 21:323–326
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