Behavioral circadian regularity at age 1 month predicts anxiety levels during school-age years

Abstract

Daily lifestyle regularity is measured using the Social Rhythm Metric (SRM). We developed a Baby SRM, with 59 babies followed for ~ 13 years. Baby SRM score at age 1 month significantly predicted the child's school (K-9, 5 time points) anxiety level (more regular = less anxious), and may be mediated through sociability and directed-attention pathways.

Introduction

Human circadian rhythm research has long been dominated by concern regarding how circadian rhythms might lead to or exacerbate psychiatric disorders such as depressive, bipolar, and anxiety disorders, when they are running at an inappropriate timing or in an irregular fashion (Wehr and Goodwin, 1983). Much of this work has been concerned with physiological circadian rhythms in body temperature, cortisol, and melatonin. However, even when behavioral circadian rhythms are considered, as measured by questionnaires and diaries, patients may have rhythms that are very different to healthy controls in their timing (Wood et al., 2009) or regularity (Shear et al., 1994), or both.

A patient's level of daily lifestyle regularity for a particular week can be measured using a diary instrument, the Social Rhythm Metric (SRM) which yields a numerical score between 0 (least regular) and 7 (most regular) (Monk et al., 1990). In healthy adults, the SRM shows an approximately Gaussian distribution with a mean at about 3.4 and a standard deviation of about 0.8 (Monk et al., 1994). High SRM scores have been shown to relate to better sleep quality and to successful aging (Monk et al., 1992, Monk et al., 2003, Carney et al., 2006), and to be protective against bereavement-related depression in widow(er)s (Prigerson et al., 1996).

In adult psychiatric illness, low SRM scores have been observed in both depressed inpatients (Szuba et al., 1992) and outpatients with anxiety disorders (Shear et al., 1994). Moreover, therapies designed to enforce greater regularity in a person's daily routine (thus increasing the SRM score) have been shown to help bipolar patients (Frank et al., 2005). Thus, underlying differences in the circadian timekeeping system driving the habitual timing of daily events may be associated with varying levels of psychopathology.

Because parents are adults with well-developed daily behavior patterns, an infant's level of circadian regularity will determine the nature of his or her interaction with them, and may thus affect early attachment relationships and the development of self-regulatory social skills in infancy. Greater infant sociability is positively related to maternal contact and responsiveness at ages 1, 3, and 9 months (Fish and Crockenberg, 1981), and secure infant attachment predicts lower levels of child and adolescent anxiety disorders (Warren, et al., 1997). Stronger and more regular circadian rhythms in the infant may increase the predictability of infant demands, leading to enhanced parental perception of need cues (Crockenberg and Leerkes, 2000) and increase parental confidence (Leerkes and Crockenberg, 2002) which might further strengthen care-taking routines. Infant social behaviors, such as smiling, are in part self-regulatory, and aid in coping with both physical and social stimulation. Mothers and fathers, whose infants exhibited significant increases in regulation and predictability from age 3 to 9 months, displayed increased sensitivity during play and greater care-taking involvement (Feldman et al., 1997). Thus, stronger and more regular circadian rhythms in the infant may enhance early parent–infant relationships and further improve infant regulatory capacity.

Temperamental rhythmicity as described by Chess and Thomas (1996) is quite similar to the current construct of Baby SRM (see below) and refers to the predictability or unpredictability in time of the sleep–wake cycle, hunger, feeding, and elimination. Children low in temperamental rhythmicity are likely to be classified as having a difficult or dysregulated temperament, and difficult or dysregulated temperament has been reliably associated with greater risk for psychopathology, including symptoms of anxiety (Rende, 1993, Warren and Simmens, 2005).

The capacity of directed-attention is a self-regulatory skill related both to cognition and emotion (Eisenberg et al., 2000). Self-regulatory and self-directed capacities are important to the development of adaptive functioning (Rothbart et al., 2000). The enhanced parent–infant and caregiver–infant relationships resulting from consolidation of an infant's alert time into daylight hours is likely to support and strengthen such self-regulation, allowing more internal resources to be devoted to environmental exploration (Ranson and Urichuk, 2008). Moreover, attentional processes may help to modulate emotional arousal (Derryberry and Reed, 1996, Rothbart et al., 2000) and to manage overt behavior when emotion is not adequately regulated by other means (Eisenberg et al., 2000). Children high in effortful control exhibit lower levels of internalizing symptoms, such as anxiety (Lengua et al., 2008). Thus, an infant's ability to direct attention may represent greater self-regulation, and is perhaps associated with stronger and more regular circadian rhythms.

Recently, major progress has been made in the field of circadian rhythms, leading to a much better understanding of the underlying mechanisms. In particular, it now appears that there are genetic polymorphisms which can determine the individual's preferred circadian phase or chronotype (Jones et al., 2007). It is also likely (though yet to be demonstrated) that there may be a genetic basis to the extent to which an individual's behavior patterns are influenced by the circadian timekeeping system, and thus the extent to which he/she is habitually regular or irregular in the timing of his/her daily events. This led to the observation (confirmed anecdotally by parents with multiple children) that from birth some babies adapt almost immediately to a 24 h routine and thus sleep through the night, while others (even within the same family) may take considerably longer. It was thus of interest to us what the level of an individual's 24 h rhythmicity in behavior might be, even as early as 1 month after birth. We thus constructed a baby analog to the adult SRM. We then related baby SRM score to the child's depression and anxiety symptoms more than a decade later, while the child was at school.