Elsevier

Neuroscience

Volume 272, 11 July 2014, Pages 217-228
Neuroscience

Individual differences in brain structure and resting-state functional connectivity associated with Type A behavior pattern

https://doi.org/10.1016/j.neuroscience.2014.04.045Get rights and content

Highlights

  • Gray matter volume of the subgenual anterior cingulate cortex positively associated with pattern A behavior scores.

  • TABP was positively correlated with increased resting-state functional connectivity between the left caudate and ventromedial prefrontal cortex.

  • TABP was also positively correlated with also increased functional connectivity between the left caudate and rostral anterior cingulate cortex.

Abstract

Type A behavior pattern (TABP) is characterized by competitiveness and hostility, time urgency and impatience. These traits can have a significant impact on physical and mental health. We have not found studies focusing on brain structure or functional connectivity correlates associated with individual differences in TABP. The present study used voxel-based morphometry (VBM) and resting-state functional connectivity (rsFC) analysis to examine the neural correlates of TABP. The results showed that TABP was positively correlated with regional gray matter volume (rGMV) in the left subgenual anterior cingulate cortex (sgACC), which might reflect immature functioning of this region related to impatience. In addition, TABP was positively correlated with the strength of rsFC between the left ventral striatum and areas in the left ventromedial prefrontal cortex (vmPFC) and the right rostral anterior cingulate cortex (rACC). These regions are associated with achievement striving related to impatience, aggressiveness, and worry under time pressure. In summary, the combination of morphometric results (increased rGMV of the left sgACC) and functional connectivity findings (increased rsFC between the left ventral caudate and the left vmPFC/right rACC in the fronto-striatal network) may provide a valuable basis for a comprehensive understanding of the neural circuitry underlying individual differences in TABP.

Introduction

According to early research, Type A behavior pattern (TABP) is an action–emotion complex characterized by time urgency and impatience (impulsiveness), competitiveness and hostility (Friedman and Rosenman, 1974, Rosenman, 1978). Specifically, TABP high scorers are described as being work-oriented, hard-driving and fast-moving individuals, who are often irritable, annoyed, impatient and aggressive (Friedman and Rosenman, 1959, Rosenman, 1978). TABP was originally identified as a constellation of emotional and behavioral characteristics (e.g., excessive and competitive drive, and an enhanced sense of time urgency) (Friedman and Rosenman, 1959, Jenkins, 1976, Glass, 1977, Rowland and Sokol, 1977, Zyzanski, 1978), which may demonstrate that TABP measures were valuable predictors of performance in academic, work and life settings. Previous studies have demonstrated the effect of TABP in university students (Barling and Charbonneau, 1992, Patel et al., 1995, Bartkus and Howell, 1999, Sato et al., 1999). Many studies found that high TABP scores were significantly correlated with depression disorder, high frustration levels and high job stress (Jamal, 1990, Sato et al., 1999, Oedegaard et al., 2006, Srivastava, 2009, Wang et al., 2011). In addition, there has been an increasing focus on the level of achievement motivation associated with inter-individual differences in TABP (Spence et al., 1987, Spence et al., 1989, Bartkus and Howell, 1999). For example, previous study has suggested that Type A behavior individuals have a higher achievement motivation orientation, and TABP might be positively related to various academic performance indices (Barling and Charbonneau, 1992). Overall, the research conducted suggests that some key dimensions of Type A behavior – for example, competitiveness (e.g., causes stress and an achievement-driven mentality), time urgency (e.g., doing something rapidly) and impatience (impulsiveness) – can predict performance outcomes and mental health (Helmreich et al., 1988). That is to say, an individual with a TABP personality trait is likely to have greater achievement output associated with a stronger sense of time urgency in all of his/her life. However, the functions of implicated structural brain regions remain unclear, as does the functional connectivity associated with individual differences in TABP. Therefore, the present study uses voxel-based morphometry (VBM) and resting-state functional connectivity (rsFC) to perform a comprehensive evaluation of the neural circuitry underlying TABP.

Though we have not found studies focusing on individual differences in brain structure and functional connectivity associated specifically with TABP, numerous studies have explored the brain structure and functional connectivity correlates of achievement striving, impulsivity – utilizing structural and functional magnetic resonance imaging (fMRI). These studies have revealed positive correlations between motivation and regional gray matter volume (rGMV) in the orbitofrontal cortex (OFC) and the striatum (Knutson et al., 2000, Breiter et al., 2001, Kirsch et al., 2003, Elliott et al., 2004, Takeuchi et al., 2014). Mizuno et al. (2008) investigated the neural activity related to academic achievement motivation, and found that the striatum was more active when subjects were highly motivated to learn (compared with control conditions), and individual activity in this area was positively correlated with the trait of academic achievement motivation. Neuroimaging research has also revealed that neuroticism (e.g., anxiety, irritation and anger) is related to brain activity in the subgenual anterior cingulate cortex (sgACC), insula and amygdala (during brain activity at rest, or in response to novel or aversive stimuli), which might be associated with irrational thinking, poor stress coping, poor impulse control and worry (Keightley et al., 2003, Etkin et al., 2004, Reuter et al., 2004, Cools et al., 2005, Eisenberger et al., 2005, Deckersbach et al., 2006, Haas et al., 2007). The sgACC in particular might be involved in conveying emotional and motivational information, and plays a key role in the automatic regulation of emotional responses (Drevets et al., 2008), including the suppression of negative emotions such as sadness and fear (Hajek et al., 2005, Drevets et al., 2008, Baeken et al., 2010, Sekiguchi et al., 2012). Another study found a positive relationship between impulsivity (a predisposition toward rapid, unplanned reactions to internal or external stimuli) and rGMV in the medial prefrontal cortex ([mPFC] including the ACC and OFC) and dorsolateral PFC, while ventral striatum volume was inversely correlated with impulsivity scores (Cho et al., 2012).

Recently, an increasing amount of research has focused on the brain anatomy associated with differences in behavior using non-invasive structural MRI (Kanai and Rees, 2011, Takeuchi et al., 2011a). Previous MRI studies in the human brain show that inter individual variability in a wide range of basic and higher cognitive functions and personality trait can be predicted from the local structure of gray and white matter as assessed by VBM or diffusion tensor imaging (DeYoung et al., 2010, Kanai and Rees, 2011). Moreover, the examination of rsFC, which reflects temporal correlations between blood oxygen level-dependent (BOLD) signals in different brain regions during rest, can indicate direct or indirect functional relations between brain regions (Friston et al., 1993, Fox and Raichle, 2007). This technique thus allows one to explore whether the brain of a TABP individual is heavily biased toward brain region connections during rest. And there is a close relationship between changes in brain structure measured using structural MRI, and changes in brain activity measured using fMRI (Kanai and Rees, 2011). As previous studies demonstrated structural abnormalities might represent a trait factor and lead to both clinical and functional changes that represent state factors (van Wingen et al., 2010, Van Wingen et al., 2011). Recent studies have found evidence for a direct relation between structural and functional connectivity. Interhemispheric resting-state functional connectivity is diminished in cases of callosal agenesis (Quigley et al., 2003) and is almost completely abolished directly after callosotomy (Johnston et al., 2008, Uddin et al., 2008). Moreover, previous studies have demonstrated the rather high stability of Type A behavior across different developmental periods between adolescence and adulthood (Jenkins, 1978, Keltikangas-Järvinen, 1989). Recent MRI studies in the human brain show that inter individual variability in a wide range of personality trait can be predicted from the local structure of gray and white matter as assessed by VBM or diffusion tensor imaging (DeYoung et al., 2010, Kanai and Rees, 2011). Thus, we applied structural imaging (VBM) first, and extracted the obtained regions as seed regions. Then, to further investigate the influence of structure changes to functional circuits, seed-based resting-state FC analysis was performed. Therefore, in the present study, we used a combined structural and rsFC analysis to examine the biological substrates of inter-individual differences in TABP.

Based on previous studies (Knutson et al., 2000, Elliott et al., 2004, Cho et al., 2012, Takeuchi et al., 2012a, Takeuchi et al., 2012b), we predicted that individual differences in TABP might be associated with rGMV variations within the PFC (e.g., the mPFC and OFC), the sgACC and the striatum. Moreover, in line with the research mentioned above, we hypothesized that inter-individual differences in TABP might be associated with rsFC in the fronto-striatal network (particularly the ventral striatum and PFC), which might be crucial for hedonic responses to rewards, and motivational and value-based learning (Schlagenhauf et al., 2009, Kehagia et al., 2010, Bjork et al., 2011). For example, some neuroimaging research have suggested that enhanced rsFC in the “money network” (including the ventromedial PFC (vmPFC), striatum, post cingulate cortex (PCC) and hippocampus, which are regions engaged in the valuation of both immediate and future rewards) is associated with increased impulsivity in economic decision making (Li et al., 2013). In addition, a recent neuroimaging study revealed that there was increased functional connectivity between the ventral striatum and the mPFC during reinforcement learning in positive compared with negative feedback conditions (van den Bos et al., 2012). Thus, we speculated that higher TABP scores (e.g., high scores for competitiveness and impulsivity) would be positively correlated with the strength of rsFC in the fronto-striatal network (i.e., for TABP individuals, the strength would be greater among the brain regions in this network).

Section snippets

Participants

In total, 329 healthy college students (152 men, mean age = 19.97 years) from Southwest University (China) participated in this study as a part of an ongoing project investigating brain imaging, creativity and mental health. Of these (329 subjects), 74 individuals were selected as TABP individuals from their total score in pattern A behavior scale (PABS), however, 13 subjects who scored 7 points on the dimension of Lie in PABS were excluded from the study. Moreover, according to the Chinese norm

Behavioral data

Table 1 shows the mean, standard deviation (SD) and range of PABS scores, and the age of each of the 60 participants. There were no significant correlations between the psychological or epidemiological measures (sex and age) and the total PABS scores.

The total score of PABS was positively correlated with depression (r = 0.35, P < 0.05). There were no statistically significant differences between men and women (P > 0.25) in terms of: the PABS total scores (mean SD for women was 29.96 ± 1.94, and for men

Discussion

To the best of our knowledge, this is the first study to investigate variations in brain structure and functional connectivity related to individual differences in TABP using a combined structural and rsFC analysis. Our results revealed a positive relationship between individual PABS scores and rGMV of the sgACC. In addition, we found that PABS score was positively correlated with the strength of rsFC between the left ventral caudate and areas in the vmPFC/rACC. Taken together, our results

Conclusion

The present study used a combined structural and rsFC analysis to examine the biological substrates of TABP. Our results showed that TABP individuals had significantly increased rGMV in the sgACC. Interestingly, functional connectivity analysis revealed enhanced strength between the left ventral striatum and areas in the vmPFC/rACC, which supported our hypothesis that fronto-striatal circuit differences were associated with individual variations in TABP, which was characterized by

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31271087), the Program for New Century Excellent Talents in University (2011) by the Ministry of Education, the Program for the Top Young Talents Chongqing, China and Chongqing Postdoctoral Science Foundation funded project (2012M510098; XM2012006). Yanqiu Wang and Jiang Qiu designed the study and wrote the protocol and manuscripts; Yanqiu Wang, Dongtao Wei and Jiang Qiu assisted with the preparation and proof-reading

References (127)

  • A. Etkin et al.

    Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces

    Neuron

    (2004)
  • T. Hahn et al.

    Neural response to reward anticipation is modulated by Gray’s impulsivity

    NeuroImage

    (2009)
  • A.A. Kehagia et al.

    Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation

    Curr Opin Neurobiol

    (2010)
  • M.L. Keightley et al.

    Personality influences limbic–cortical interactions during sad mood induction

    NeuroImage

    (2003)
  • P. Kirsch et al.

    Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study

    NeuroImage

    (2003)
  • B. Knutson et al.

    FMRI visualization of brain activity during a monetary incentive delay task

    NeuroImage

    (2000)
  • K. Mizuno et al.

    The neural basis of academic achievement motivation

    NeuroImage

    (2008)
  • G. Northoff et al.

    Cortical midline structures and the self

    Trends Cogn Sci

    (2004)
  • K.J. Oedegaard et al.

    Type A behaviour differentiates bipolar II from unipolar depressed patients

    J Affect Disord

    (2006)
  • M. Patel et al.

    Type A behaviour and the perception of facially expressed affect

    Personality Individ Differ

    (1995)
  • M.L. Phillips et al.

    Neurobiology of emotion perception I: the neural basis of normal emotion perception

    Biol Psychiatry

    (2003)
  • G.J. Quirk et al.

    Prefrontal mechanisms in extinction of conditioned fear

    Biol Psychiatry

    (2006)
  • A. Rangel et al.

    Neural computations associated with goal-directed choice

    Curr Opin Neurobiol

    (2010)
  • G.R. Ridgway et al.

    Issues with threshold masking in voxel-based morphometry of atrophied brains

    NeuroImage

    (2009)
  • M. Rushworth et al.

    Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour

    Trends Cogn Sci

    (2007)
  • N. Sato et al.

    Subjective mental workload in type A women

    Int J Ind Ergon

    (1999)
  • F. Schlagenhauf et al.

    Reward feedback alterations in unmedicated schizophrenia patients: relevance for delusions

    Biol Psychiatry

    (2009)
  • M. Song et al.

    Brain spontaneous functional connectivity and intelligence

    Neuroimage

    (2008)
  • J. Abutalebi et al.

    Bilingualism tunes the anterior cingulate cortex for conflict monitoring

    Cereb Cortex

    (2012)
  • D.M. Amodio et al.

    Meeting of minds: the medial frontal cortex and social cognition

    Nat Rev Neurosci

    (2006)
  • B.W. Balleine et al.

    Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action

    Neuropsychopharmacology

    (2009)
  • J. Barling et al.

    Disentangling the relationship between the achievement striving and impatience—irritability dimensions of type A behavior, performance and health

    J Organizational Behav

    (1992)
  • K.R. Bartkus et al.

    The relative influence of achievement motivation and irritability-impatience on the selling performance of travel agents: implications of the type A behavior pattern

    J Travel Res

    (1999)
  • A. Bechara et al.

    Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making

    J Neurosci

    (1999)
  • H. Berlin et al.

    Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions

    Brain

    (2004)
  • J.A. Blumenthal et al.

    Type A behavior pattern and coronary atherosclerosis

    Circulation

    (1978)
  • M. Botvinick et al.

    Conflict monitoring versus selection-for-action in anterior cingulate cortex

    Nature

    (1999)
  • Z. Boyuan

    Psychophysiological reaction in cardiovascular disease: II. A study on the behavior pattern of coronary heart disease patients [J]

    Acta Psychol Sin

    (1985)
  • D.M. Bryant et al.

    Neuroanatomical phenotype of Klinefelter syndrome in childhood: a voxel-based morphometry study

    J Neurosci

    (2011)
  • R.L. Buckner et al.

    The brain’s default network

    Ann N Y Acad Sci

    (2008)
  • Y. Chao-Gan et al.

    DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI

    Front Syst Neurosci

    (2010)
  • R. Cools et al.

    Individual differences in threat sensitivity predict serotonergic modulation of amygdala response to fearful faces

    Psychopharmacology

    (2005)
  • J.L. Cummings et al.

    The neuropsychiatric inventory comprehensive assessment of psychopathology in dementia

    Neurology

    (1994)
  • T. Deckersbach et al.

    Regional cerebral brain metabolism correlates of neuroticism and extraversion

    Depression and anxiety

    (2006)
  • M. Delgado et al.

    Motivation-dependent responses in the human caudate nucleus

    Cereb Cortex

    (2004)
  • T.M. Dembroski et al.

    Physiologic reactions to social challenge in persons evidencing the type A coronary-prone behavior pattern

    J Hum Stress

    (1977)
  • C.G. DeYoung et al.

    Testing predictions from personality neuroscience brain structure and the big five

    Psychol Sci

    (2010)
  • A. Di Martino et al.

    Functional connectivity of human striatum: a resting state FMRI study

    Cereb Cortex

    (2008)
  • E.K. Diekhof et al.

    Impulsive personality and the ability to resist immediate reward: an fMRI study examining interindividual differences in the neural mechanisms underlying self-control

    Hum Brain Mapp

    (2012)
  • W.C. Drevets et al.

    Subgenual prefrontal cortex abnormalities in mood disorders

    Nature

    (1997)
  • Cited by (10)

    • RELN rs7341475 Associates with Brain Structure in Japanese Healthy Females

      2022, Neuroscience
      Citation Excerpt :

      As our sample consisted of healthy females without a diagnosis of mental illness, the enlargement of rGMV in ACC in subjects with the SZ risk genotype may indicate the action of this protective mechanism. Conversely, previous studies have reported that an increase in the rGMV in the ACC is associated with various personality traits such as empathy (Banissy et al., 2012), mindfulness (Lu et al., 2014), narcissistic personality (Nenadić et al., 2021), type A behavior pattern (Wang et al., 2014), internal locus of control (Hashimoto et al., 2015), extraversion (Kapogiannis et al., 2013), self-handicapping tendency (Takeuchi et al., 2013), a need for uniqueness (Takeuchi et al., 2012), internet addiction tendency (Li et al., 2015), and effortful control (Zhang et al., 2015). Therefore, enlargement of the ACC rGMV as protection against SZ development in G/G homozygotes could be a secondary mechanism that contributes to these personalities.

    • Altered gray matter density and disrupted functional connectivity of the amygdala in adults with Internet gaming disorder

      2015, Progress in Neuro-Psychopharmacology and Biological Psychiatry
      Citation Excerpt :

      Both GMD and FC were evaluated in a wide variety of psychiatric conditions (Yang et al., 2013; Yi et al., 2012), including addictions (Ide et al., 2014; Liao et al., 2011; Zhang et al., 2014a). Combined evaluation could assess the compatibility difference in both brain structure and FC (Qin et al., 2014; Wang et al., 2014). For example, an abnormal structure or function of the amygdala is a common component of neurodevelopmental disorders (Schumann et al., 2011).

    View all citing articles on Scopus

    Equal contribution.

    View full text