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