Personality—an individual’s habitual pattern of cognition, emotion, and behaviour—is relatively stable and enduring (Endler, 2000
). However, it is not entirely fixed throughout the lifespan, but is more likely to fluctuate during certain developmental phases such as early and late adulthood (Roberts, Walton, & Viechtbauer, 2006
). These changes may be influenced in part by genetic predispositions (McCrae et al., 2000
) or by environmental influences such as life experiences and age-related role expectations (Roberts & Caspi, 2003
). Continuous changes in brain structure and function that occur throughout life also likely play a significant role. Accordingly, in people with brain injury or neurodegenerative disease, dramatic changes in personality can rapidly overcome established premorbid personality traits.
Studies measuring personality traits in a variety of neurodegenerative diseases such as frontotemporal dementia (FTD), Alzheimer’s disease (AD), and dementia with Lewy bodies (DLB) found that patients` social behaviours and personality traits change markedly relative to their premorbid state (Chatterjee, Strauss, Smyth, & Whitehouse, 1992
; Galvin, Malcom, Johnson, & Morris, 2007
; Rankin, Baldwin, Pace-Savitsky, Kramer, & Miller, 2005
). FTD and AD patients demonstrated quantitative differences in degree and type of personality change (Chatterjee et al., 1992
; Rankin, Kramer, Mychack, & Miller, 2003
). The mildly increased introversion and submissiveness seen early in AD patients may be a realistic response to loss of cognitive capacity, rather than a direct effect of damage to social and emotional circuits in the brain, however, in FTD patients, personality changes relative to patients` premorbid state such as early decline in social interpersonal conduct and early impairment in regulation of personal conduct are core diagnostic features (Neary et al., 1998
), and appear to directly result from brain damage. When FTD patients are grouped according to whether their atrophy is predominantly frontal or temporal, they show very different patterns of personality change (Rankin et al., 2003
). The different patterns of personality change in different neurodegenerative diseases imply relationships between personality traits and brain structures.
Support for personality-brain structure relationships comes from a small study, which has linked FTD patients’ diminished agreeableness to volume loss in the right orbitofrontal cortex (Rankin et al., 2004
). However, elucidation of the neural networks underlying different personality traits requires a more large-scale, detailed, whole-brain analysis in patients with divergent neurodegenerative diseases.
In this study, we hypothesized that specific interpersonal traits would correspond to anatomic changes in patients with various neurodegenerative diseases. To examine this hypothesis, we correlated quantitative measures of eight interpersonal traits using the Interpersonal Adjective Scales (IAS) () with structural MR images using voxel-based morphometry (VBM) across the whole brain in a large cohort of subjects. The IAS circumplex, which is defined by the two dimensions of extraversion and agreeableness of the five-factor model (McCrae & Costa, 1989
), was chosen, because we were most interested in the interpersonal and social dimensions of personality. We hypothesized that neural networks underlying interpersonal traits would be organized along three spatial gradients in the brain: a ventro-dorsal, a medio-lateral, and a right-left gradient ().
The Interpersonal Circumplex of the Interpersonal Adjective Scales. Eight interpersonal traits, derived from two orthogonal dimensions, agency and affiliation, are evenly distributed around the circumference.
Figure 2 Schematic anatomical organization of the three hypothesized spatial gradients of the brain: the ventro-dorsal (Hypothesis 1), the medio-lateral (Hypothesis 2), and the right-left (Hypothesis 3) gradient, displayed on a rendered standard brain from a single (more ...)
These three spatial gradients are derived from existing models and meta-analyses of neuroimaging and electrophysiological studies of cognition, emotion, and social behaviour in humans and non-human primates. First, the ventro-dorsal gradient is clinically characterized by a continuum between more automatic, emotional, and stimulus-driven behaviour, mediated by more ventral prefrontal regions, versus more controlled, reflective behaviour, originating in more dorsal prefrontal regions (Amodio & Frith, 2006
; Lieberman, 2007
; Olsson & Ochsner, 2008
; Phillips, Drevets, Rauch, & Lane, 2003
). With respect to personality, therefore, we expected that traits involving emotionally affiliative behaviours such as warmth and ingenuousness () would correlate predominantly with ventral prefrontal regions. Traits high in personal agency such as dominance and arrogance would correlate predominantly with dorsal prefrontal regions. Extraversion, a trait high in both emotional affiliation and personal agency, would probably have neural correlates in both ventral and dorsal prefrontal regions.
Second, the medio-lateral gradient is clinically characterized by a continuum between internally-focused processes, including emotions and thoughts, mediated by more medial fronto-parietal regions, versus more externally-focused, task-oriented, and controlled processes, originating in more lateral fronto-temporo-parietal regions (Koechlin, Ody, & Kouneiher, 2003
; Lieberman, 2007
; Northoff et al., 2006
; Olsson & Ochsner, 2008
; Tanji & Hoshi, 2008
). Thus with regard to personality, we expected that traits involving higher levels of affiliation such as warmth or traits involving higher levels of internal orientation such as introversion would relate predominantly to midline fronto-parietal structures. Agentic traits involving higher levels of external orientation such as dominance, which reflects the tendency to negotiate with one’s environment to accomplish personal goals, and extraversion were expected to correlate with lateral fronto-temporo-parietal structures.
Finally, our hypothesis that there would be a right-left gradient to some personality traits draws support from three complementary models of brain lateralization: the right-hemisphere model, the dominance/submission model, and the approach/withdrawal model (e. g., Demaree, Everhart, Youngstrom, & Harrison, 2005
). The right-hemisphere model, which is mainly based on human lesion studies, posits that the right hemisphere is specialized for the perception and expression of emotions (Adolphs, 2002
; Borod, Bloom, Brickman, Nakhutina, & Curko, 2002
; Demaree et al., 2005
). With respect to personality, therefore, we expected that emotionally affiliative traits would be more likely to lateralize to the right hemisphere. Taken together, the dominance/submission and approach/withdrawal models suggest a left-lateralization for interpersonal dominance and approach behaviours, and right-lateralization for interpersonal submissiveness and withdrawal behaviours. Thus we expected that assertive, approach-related traits such as dominance and extraversion predominantly would be mediated by the left forebrain, whereas more interpersonally passive traits such as submissiveness and ingenuousness would relate to the right forebrain. Because extraversion involves both agentic and affiliative aspects, these three models suggest it would draw upon circuitry in both the left (agentic) and right (affiliative) hemispheres.