Elsevier

Neuroscience

Volume 217, 16 August 2012, Pages 77-83
Neuroscience

Individual differences in trait anxiety are associated with white matter tract integrity in the left temporal lobe in healthy males but not females

https://doi.org/10.1016/j.neuroscience.2012.05.017Get rights and content

Abstract

The temporal lobe plays a major role in anxiety and depression disorders and is also of importance for trait anxiety in the non-pathological range. The present study investigates self-report data of personality dimensions linked to trait anxiety in the context of white matter tract integrity in the temporal lobes of the human brain in a large sample of N = 110 healthy participants. The results show that especially in men values for fractional anisotropy of several white matter tracts in the temporal lobe of the left hemisphere correlate substantially with individual differences in trait anxiety (depending on the tract investigated between .40 and .49). The present study shows that not only data from functional magnetic resonance imaging (fMRI), but also from structural diffusion tensor imaging (DTI) provide interesting insights into the biological foundation of human personality traits.

Highlights

► The present study investigates trait anxiety by means of DTI. ► The study links white matter integrity of the temporal lobe to trait anxiety in humans. ► The association between FA values and anxiety can be observed in males only.

Introduction

In the last years not only functional but also structural imaging of the brain helped to illuminate the biological underpinnings of personality traits linked to negative emotionality. One of the main focuses of biologically oriented personality research was among others the hippocampus structure, which is hypothesized to play a key role for trait anxiety (Gray and McNaughton, 2000). This idea found support in structural brain imaging studies such as by Yamasue et al. (2008) who linked smaller hippocampus volumes in the right hemisphere to higher Harm Avoidance scores in both males and females. DeYoung et al. (2010) investigated the BIG 5 personality dimensions with structural imaging and showed that the anxiety linked trait Neuroticism was linked to reduced brain matter volume in the left medial temporal lobe including parts of the posterior hippocampus. Studies investigating different patient populations linked lower hippocampus volume to generalized social phobia (Irle et al., 2010), depression (Sheline, 2011) and vulnerability for posttraumatic stress disorders (Pitman et al., 2001). Besides the hippocampus also the amygdala has been associated with anxiety. This is not surprising, because both structures are closely entwined. Among others studies linked lower amygdala volumes to panic disorder (Hayano et al., 2009), financial hardships (Butterworth et al. in press) and higher Neuroticism scores (Omura et al., 2005). In general, inconsistencies exist in the field showing both negative (as shown) and positive correlations between anxiety and hippocampus/amygdala volume (e.g. Barrós-Loscertales et al., 2006, Cherbuin et al., 2008, Schienle et al., 2011). Given the importance of the hippocampus formation and its adjacent area for trait anxiety and associated psychopathological disorders, the present study seeks to investigate white matter tract integrity of the tracts linking the hippocampus to other structures of the human brain in the context of personality measures of trait anxiety. Such an endeavor has been made possible by the development of diffusion tensor imaging (DTI) that provides scalar indices such as fractional anisotropy (FA) to characterize white matter tract integrity. In a first study by Cohen et al. (2009) DTI has been applied to investigate possible links between personality and structural connectivity of the human brain. They could show that fiber tracts between a subcortical network, including the hippocampus and the amygdala, and the ventral striatum predicted individual differences in Novelty Seeking while tracts between prefrontal cortex and the striatum predicted individual differences in Reward Dependence. However, in this study connectivity-based parcellation and tractography were used, FA analysis showed no significant results. Another interesting study by Kim and Whalen (2009) investigated DTI tracts to show associations with trait anxiety measured with Spielberger’s Trait Anxiety Inventory (STAI-T). They showed that white matter tract integrity was inversely correlated with anxiety in a tract linking the ventromedial prefrontal cortex with the amygdala. Another study warrants attention in the context of personality and FA values: Westlye et al. (2011) also provided evidence for an inverse relationship between FA values and Harm Avoidance in several tracts of the cortico-limbic circuitry. In the present study we chose the temporal lobe as a region of interest to investigate the white matter tract integrity and its link to the biologically oriented personality measures of trait anxiety as defined by Cloninger et al., 1993, Gray and McNaughton, 2000 and Eysenck and Eysenck (1991).

Given the findings by Kim and Whalen (2009) and Westlye et al. (2011) one might hypothesize an inverse correlation between FA values and trait anxiety in the tracts under investigation. In line with this hypothesis, another study investigating patients of social anxiety disorder and healthy controls reported lower FA values in the right uncinate fasciculus (UF) in the patient group (Phan et al., 2009). However, there is also some evidence contrary to this hypothesis. A recent study by Blood et al. (2010) demonstrated that also higher FA values might be associated with negative emotionality: FA values in the ventral tegmental area were higher in a group of depressed patients compared to healthy controls. Moreover, trait anxiety was reported to be higher in patients with abnormal ventral tegmental areas. A study by Zhang et al. (2012) on post-traumatic stress disorder showed higher FA values in the posterior cingulate gyrus (PCG), but again, as reported earlier – a negative correlation between PCG and trait anxiety appeared. The heterogeneity of DTI findings in the context of anxiety has been pointed out in detail in a recent review article on DTI and anxiety disorders by Ayling et al. (2012). Given the inconsistencies of these findings, it is difficult to derive a directed hypothesis for the present study. Therefore, we did not set up a directed hypothesis with respect to the association between trait anxiety and FA values.

Section snippets

Participants

N = 110 healthy participants filled in three personality questionnaires measuring individual differences in negative emotionality (for details see below). N = 44 participants were male and n = 66 participants were female (mean age = 29.04, SD = 10.94). A current or past neurological/psychiatric disorder led to exclusion from the study. All participants gave their written informed consent. The study was approved by the medical ethics committee of the University of Bonn, Germany.

Personality self-report

Three different

Personality measures, age and gender

The personality measures under investigation are highly intercorrelated so that they show a considerable overlap (ranging from r = .57 (p < .01) between BIS and Harm Avoidance and r = .55 (p < .01) between Neuroticism and BIS to r = .73 (p < .01) between Harm Avoidance and Neuroticism). Because of these high correlations, we extracted one factor called “trait anxiety” (negative emotionality) with an Eigenvalue of 2.23 explaining 74.38% of the variance by using a PCA. This approach has been applied before

Discussion

DTI represents an important tool to investigate the structural connectivity of the human brain. Most of the studies used DTI to illuminate the neuronal basis of neurological or psychopathological disorders until now. But this imaging technique is also of importance to investigate the biological underpinnings of human personality. Because research has focused on the role of the hippocampus/amygdala in clinical anxiety and depression and also in explaining individual differences in anxiety (e.g.

Conclusions

Summing up, the present study shows that trait anxiety is positively correlated with FA values of several white matter tracts connecting the hippocampus with diverse regions of the human brain in males but not females. Therefore, it is of importance to consider “sex” as an important variable in the investigation of trait anxiety and white matter tract integrity. Moreover, “healthy” anxiety is an important emotion promoting survival in situations of high uncertainty. Here, higher tract integrity

Conflict of Interest

None.

Contributions

CM and JCS designed the study, analyzed the data and prepared the manuscript. MR, BW and SM analyzed the data and prepared the manuscript.

Acknowledgements

JCS was supported by the Gerok Programme of the BONFOR commission, University of Bonn. BW was supported by a Heisenberg Grant of the DFG (Deutsche Forschungsgemeinschaft). The study was additionally partly supported by the “Verein zur Foerderung der Epilepsieforschung Bonn”.

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