Regional gray matter density is associated with morningness–eveningness: Evidence from voxel-based morphometry

Highlights

• Morningness associated with lower regional gray matter density (rGMD) in precuneus

• Morningness associated with lower rGMD in the left posterior parietal cortex

• Morningness associated with higher rGMD in the bilateral orbitofrontal cortex

• Morningness associated with higher rGMD in the bilateral suprachiasmatic nuclei

Abstract

Diurnal preference (morningness–eveningness) is known to be associated with several individual characteristics that are important in the fields of sociology, education, and psychiatry. Despite this importance, the anatomical correlates of individual differences in morningness–eveningness are unknown, and these were investigated in the present study. We used voxel-based morphometry and a questionnaire to determine individual morningness–eveningness and its association with brain structures in 432 healthy men and 344 healthy women (age, 20.7 ± 1.8 years). We demonstrated that morningness (less eveningness) was associated with (a) lower regional gray matter density (rGMD) in the precuneus and adjacent areas, (b) lower rGMD in the left posterior parietal cortex and adjacent areas, and (c) higher rGMD in the bilateral orbitofrontal cortex. Further, our exploratory analyses revealed that (d) higher rGMD in hypothalamic areas around the bilateral suprachiasmatic nuclei were associated with morningness. These findings demonstrate that variations in morningness–eveningness reflect the GM structures of focal regions across the cortex, and suggest a structural basis for individual morningness–eveningness and its association with a wide range of psychological variables distributed across different GM areas of the brain.

Introduction

The continuum of diurnal preference or “morningness–eveningness” refers to individual differences in the timing of circadian sleep–wake cycles and subjective alertness throughout the day (Killgore and Killgore, 2007). It has been suggested that approximately 50% of individual variability in morningness–eveningness is affected by genetic factors (Hur and Lykken, 1998) including polymorphisms in circadian clock-relevant genes (Takahashi et al., 2008), suggesting the robust innate basis of this measure. The negative feedback loops associated with the expression of these genes form the circadian rhythm (e.g., Darlington et al., 1998, Jin et al., 1999) and polymorphisms in these genes affect the length of circadian rhythms (e.g., Katzenberg et al., 1998). These genes are widely expressed, but particularly enriched in the suprachiasmatic nucleus, and neuronal activity in this area plays a central role in coordinating circadian rhythms (Inouye and Kawamura, 1982). Performance and neural activity changes in this area, which are related to interactions between time of day and morningness–eveningness, have been previously investigated in humans (Schmidt et al., 2009).

There are several measurements of morningness–eveningness. One of the representative meth The most widely used instrument is the Morningness–Eveningness Questionnaire (MEQ), which is a self-report measure (Horne and Ostberg, 1976). We focused on this scale as a method to measure morningness-eveningness in this study. This scale contains questions about feelings and behaviors that are related to sleep, peak performance, and other circadian functions. The reliability of MEQ, as measured by Cronbach's coefficient of alpha was .89. Moreover, MEQ has been shown to be a valid indicator of circadian arousal (Smith et al., 1989), and a higher MEQ score has been shown to be associated with an earlier time of the lowest body temperature (Baehr et al., 2000) as well as an earlier time of waking (Baehr et al., 2000) and a shorter intrinsic circadian period (Duffy et al., 2001), as predicted theoretically. These findings demonstrate the criterion-related validity of the test. In addition, it should be noted that the MEQ score and the concept of morningness–eveningness reflect not only circadian processes but also homeostatic processes (Mongrain et al., 2006). For example, subjects with morningness tend to show faster dissipation of sleep pressure during sleep, while buildup of sleep pressure during wakefulness is slower in subjects with eveningness (Mongrain et al., 2006, Taillard et al., 2003).

On the other hand, it is also well established that there is another aspect to individual characteristics of morningness–eveningness that exists regardless of the time of day. First, morningness–eveningness has been associated with biological factors such as sex (Adan and Natale, 2002) and age (Randler and Saliger, 2011). These are biological factors that are likely to affect morningness–eveningness. Morningness has also been associated with personality and temperament, especially cognitive components associated with self-discipline and pro-social behaviors such as high conscientiousness, high self-directedness, low impulsiveness, and high cooperativeness and agreeableness (Lee et al., 2012, Randler, 2008, Randler and Saliger, 2011). At least some of these factors, particularly those related to discipline, may be associated with morningness because a well-disciplined lifestyle may lead to morningness (Díaz-Morales et al., 2008). Second, eveningness has been associated with greater higher-order cognitive abilities such as higher psychometric intelligence and higher working memory capacity even when these are assessed in the morning (Piffer et al., 2014, Roberts and Kyllonen, 1999) despite low academic performance (Díaz-Morales and Escribano, 2013, Randler and Frech, 2006). The causal mechanisms underlying these associations are not clear; however, one speculation is that a third factor such as the basic arousal level leads to both higher cognitive abilities and eveningness. Third, eveningness has been associated with traits or states linked to worse mood such as higher harm avoidance, higher neuroticism, and more suicide attempts (Lee et al., 2012, Randler, 2008, Randler and Saliger, 2011, Selvi et al., 2011). These may partly be consequences of eveningness in modern life. For example, eveningness is associated with insufficient sleep (Taillard et al., 1999), which in turn may lead to a chronic bad affective state (Akashiba et al., 2002). In addition, insufficient sleep and the fact that tests and classes are held earlier in the day at school may underlie the low academic performance (Díaz-Morales and Escribano, 2013), which in turn may lead to a bad affective state. These emotional problems in eveningness may underlie their low pro-sociality, which is described above, because well-being and pro-sociality have a close positive relationship (Strayer and Roberts, 2004, Takeuchi et al., 2014a). Finally, perhaps because of sleep and emotional problems, eveningness has also been associated with attentional and behavioral problems in everyday life (Baird et al., 2012, Gau et al., 2007, Susman et al., 2007).

Thus, morningness–eveningness is an essential characteristic of individuals. It is related to a wide range of individual characteristics that are important in society, education and clinical areas such as academic performance, aging, sex, and traits and states associated with psychiatric disorders and social cognition. However, despite the unique importance of the morningness–eveningness construct, the anatomical basis of the aspects of morningness–eveningness that are related to a wide range of stable abilities and traits of individuals is unknown.

We hypothesized that increased morningness is associated with the following various brain structures in young adults by considering the wide range of psychological correlates of morningness–eveningness. (A) Less gray matter (GM) structures in the precuneus, medial prefrontal cortex, and adjacent regions, which are structurally associated with pro-social (Banissy et al., 2012, Coutinho et al., 2013, Hu et al., 2011, Takeuchi et al., 2014b) and self-disciplinary cognitive components (Gardini et al., 2009, Takeuchi et al., 2011f) and functionally associated with inference of mind, both of one's own mind and that of others (Ochsner et al., 2004); (B) larger or less GM structures in the anterior brain regions including the medial prefrontal cortex, orbitofrontal cortex (OFC), lateral prefrontal cortex, and anterior cingulate cortex, which are associated with higher-order cognitive functions; (C) less GM structures in areas associated with states or traits linked to negative mood, such as the amygdala/hippocampal areas (Iidaka et al., 2006, Yamasue et al., 2008), insula (Takeuchi et al., 2014b); (D) larger GM structures in some of the abovementioned areas and the posterior parietal cortex (PPC), which are liked to attentional problems in everyday life (Kanai et al., 2011).

To test these hypotheses, we investigated how individual differences in morningness–eveningness were associated with regional GM density (rGMD) using voxel-based morphometry (VBM) (Good et al., 2001) after controlling for age, sex, general intelligence, and total intracranial volume.

As described in our previous study (Takeuchi et al., 2012c), functional imaging and structural studies have advantages and disadvantages, and they can be useful in different situations. Here, structural imaging studies are especially useful for investigating the aspects of morningness–eveningness that are related to a wide range of stable abilities and traits of individuals. This is because unlike the results of functional magnetic resonance imaging (fMRI) studies, the results of structural imaging studies are not likely to be affected by the time of day. Furthermore, in MRI correlation studies (including those of fMRI) that investigated the neural basis of individual differences, we are able to use established cognitive measures with proven reliability and validity to tap individual differences in cognition. As summarized in our previous study (Takeuchi et al., 2012b), GM in VBM is thought to reflect the number and size of neurons and glial cells, the synaptic bulk, and the number of neurites (May and Gaser, 2006, Takeuchi et al., 2011e). However, this idea remains to be proven by histological studies. The rGMD has also been associated with specific individual personality (trait) characteristics (e.g., Haier et al., 2004, Kanai et al., 2011, Takeuchi et al., 2010a, Takeuchi et al., 2013c). Structural imaging thus provides unique information about the neural origin of morningness–eveningness. Automated VBM yields data comparable to that of manual region of interest (ROI)-based analyses (Testa et al., 2004). Recent advancement of preprocessing methods, including segmentation using more tissue classes, and diffeomorphic anatomical registration using diffeomorphic anatomical registration through exponentiated lie algebra (DARTEL) methods have further improved the accuracy of results and achieved more precise inter-subject registration of brain images (Klein et al., 2009, Peelle et al., 2012).