The Degree of Early Life Stress Predicts Decreased Medial Prefrontal Activations and the Shift from Internally to Externally Guided Decision Making: An Exploratory NIRS Study during Resting State and Self-Oriented Task

Takashi Nakao,Daisuke Shimizu,Shigeto Yamawaki,Yasumasa Okamoto,Shigeru Morinobu,Georg Northoff,Tomoya Matsumoto,Shinpei Yoshimura,Machiko Morita

doi:10.3389/fnhum.2013.00339

Abstract

Early life stress (ELS), an important risk factor for psychopathology in mental disorders, is associated neuronally with decreased functional connectivity within the default mode network (DMN) in the resting state. Moreover, it is linked with greater deactivation in DMN during a working memory task. Although DMN shows large amplitudes of very low-frequency oscillations (VLFO) and strong involvement during self-oriented tasks, these features’ relation to ELS remains unclear. Therefore, our preliminary study investigated the relationship between ELS and the degree of frontal activations during a resting state and self-oriented task using near-infrared spectroscopy (NIRS). From 22 healthy participants, regional hemodynamic changes in 43 front-temporal channels were recorded during 5 min resting states, and execution of a self-oriented task (color-preference judgment) and a control task (color-similarity judgment). Using a child abuse and trauma scale, ELS was quantified. We observed that ELS showed a negative correlation with medial prefrontal cortex (MPFC) activation during both resting state and color-preference judgment. In contrast, no significant correlation was found between ELS and MPFC activation during color-similarity judgment. Additionally, we observed that ELS and the MPFC activation during color-preference judgment were associated behaviorally with the rate of similar color choice in preference judgment, which suggests that, for participants with higher ELS, decisions in the color-preference judgment were based on an external criterion (color similarity) rather than an internal criterion (subjective preference). Taken together, our neuronal and behavioral findings show that high ELS is related to lower MPFC activation during both rest and self-oriented tasks. This is behaviorally manifest in an abnormal shift from internally to externally guided decision making, even under circumstances where internal guidance is required.

Highlights

By definition, early life stress (ELS) derives from adverse experiences during childhood and adolescence including physical, sexual, and maltreatment abuse (Brown et al, 2009)
A clear distinction between early and recent life stress, measurement of ELS in child abuse and trauma scale (CATS), is not confounded by recent life stress (LES). Both CATS (r = −0.04, p = 0.87, confidence intervals (CI) = −0.43 to 0.38) and life event stress scale (LES) (r = 0.15, p = 0.51, CI = −0.30 to 0.45) scores were not correlated with cortisol levels, suggesting that both early and recent life stress was not associated with the cortisol level, the elevation of which can alter the medial prefrontal cortex (MPFC) activity
These relations were observed only in the similarity-easy set trials, which suggests that participants who showed high ELS and decreased MPFC activation during the self-oriented task tend to make decisions based on a salient external criterion during the task, which requires decisions based on their own internal criteria

Summary

Introduction

Early life stress (ELS) derives from adverse experiences during childhood and adolescence including physical, sexual, and maltreatment abuse (Brown et al, 2009). ELS is associated with deficits in cognitive and affective function (Pechtel and Pizzagalli, 2011) and is a significant risk factor for mood and anxiety disorders later in life (Heim and Nemeroff, 2001; Heim et al, 2010; Schmidt et al, 2011). Reports of some animal studies have described that ELS results in abnormally increased synaptic density in the infralimbic cortex (Ovtscharoff and Braun, 2001), and decreased dendritic spine density in the prefrontal cortex (PFC) (Murmu et al, 2006). Reports of human neuroimaging studies have described that ELS is associated with reduced gray matter volume including that of the PFC (De Bellis et al, 2002; Andersen et al, 2008; Paus et al, 2008; Hanson et al, 2010). The DMN consists mainly of cortical midline structures (Northoff and Bermpohl, 2004; Raichle and Gusnard, 2005) and comprises the medial prefrontal

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