Effects of constant daylight exposure during early development on marmoset psychosocial behavior

https://doi.org/10.1016/j.pnpbp.2011.01.008Get rights and content

Abstract

Due to global industrialization, the light cycle is shifting to longer daytime. Mounting evidence indicates that social developmental disorders may correlate with longer periods of daytime in childhood. However, the exact mechanisms of this link remain unclear. To examine the impact of longer day-time on psychosocial development, we developed a novel non-human primate model, using the common marmoset (Callithrix jacchus) reared under constant daylight from birth. Marmosets were reared individually by human nursing under constant light (LL) during varying periods in juvenile development, and their behaviors were compared with those of normal day–night cycle (LD) marmosets by multivariate analysis based on principal component analysis (PCA). LL marmosets elicited egg-like calls (e-call) less in juvenile period, and displayed side-to-side shakes of the upper body with rapid head rotation through adulthood frequently. Based on the PCA, these behaviors were interpreted as ‘alert’ or ‘hyperactive’ states. Additionally, behavioral development of marmosets reared under constant dark (DD) was markedly different from both LD and LL marmosets, suggesting the fundamental importance of daylight-dependent neuronal and endocrine processes and entrainment by a constant 24-hour light/dark cycle on psychosocial behavior development.

Research Highlights

► The psychobehavioral development of primates affected by constant daylight exposure. ► Behavioral multivariate and regression analysis from juveniles to adults longitudinally. ► Early constant light resulted in alert and hyperactive tendency in adolescent primates.

Introduction

Disturbances of circadian rhythm due to abnormal lighting conditions may be involved in the pathogenesis of various psychiatric disorders, such as insomnia, depression, and mental maldevelopment (Germain and Kupfer, 2008, Kohyama, 2009, Lewy, 2007), presumably through neuronal and hormonal mechanisms regulating sleep, temperature, and mood cycles (Bunney and Potkin, 2008). Animal research has confirmed the importance of circadian rhythms for hormonal and behavioral functioning (Cambras et al., 1998, Connolly et al., 1983, Diez-Noguera and Cambras, 1990, Mistlberger and Skene, 2004, Schelstraete et al., 1992, Toki et al., 2007, Yerushalmi et al., 2006). Recent animal studies examined the development of circadian rhythm itself, as well as the relationship between circadian rhythm and socio-emotional behavior in two ways: the effect of social zeitgeber (time-cue) on circadian timing, and the effect of circadian rhythm on socio-emotional behavior (Mistlberger and Skene, 2004, Toki et al., 2007). However, the direct effect of abnormal circadian rhythms in early life on social behavior development is difficult to study due to the tight mother–infant interaction in mammalian models (Schelstraete et al., 1992, Toki et al., 2007). To examine the impact of longer day-time on psychosocial development, we have developed a novel common marmoset (Callithrix jacchus) model in which the subjects were fed milk by humans until weaning, and then isolated from other marmosets to simplify the social experience. In this experimental setup, we were able to examine directly the effects of early atypical light zeitgeber on psychological behavior in social contexts. Furthermore, we have developed a new approach to quantify and detect the subtle differences of complex psychological behaviors using a multi-parametric visualization of social interaction based on principal component analysis (we named as ‘Bouquet analysis’).

In this study, subjects were raised individually by human nursing for several months from birth under either normal (12 h light:12 h dark cycle; LD) or constant light (LL) conditions, or as another extreme condition, constant dark (DD). From the video recordings over the developmental time period (postnatal days 30–440), behavior parameters were extracted and assessed by principal component analysis (PCA). We found that LL group had subtle but important features in the one call type associated with seeking alert that could be visualized as a unique developmental pattern in each group through adolescence and adulthood. These results suggest that circadian rhythms in early life affect psychosocial development persisting through adulthood.

Section snippets

Animals

The experimental protocols were approved by the Animal Care and Use Committee of the Tokyo Metropolitan Institute for Neuroscience. Immediately after birth, marmoset babies were isolated from their parents, and were fed on milk until weaning. They were housed individually in transparent plastic cages (22 × 14 × 14 cm) with paper sheets on the cage floor. Each cage was placed in a light-sealed incubator illuminated by a fluorescent lamp maintaining constant temperature (32 °C). Approximately 25 days

Effect of lighting condition on early arrhythmicity and later free run-rhythm

The responses of experimental animals are presented in Fig. 1d–f. A rest-activity rhythm was recorded and the day–night rhythm in LD appeared around day 30 (P30d) and was well entrained by a 12-hour light/dark cycle. On the other hand, the rhythm in LL as well as DD conditions appeared as free-run patterns. In all conditions, arrhythmic period was present during early development.

Difference in behavior development trajectory between LD and LL-conditioned marmosets

To examine the impact of photic experience during early development of marmoset locomotion rhythm and social

Discussion

Here we developed a new method to quantify behavior in social contexts, the Behavior Output analysis for Quantitative Emotional state Translation (Bouquet analysis), to examine the effects of constant light exposure during early life on marmoset behavior throughout their development. To consider the practical model of normal human development, LD was assumed as the control group to be compared with LL and DD cohorts. The latter marmosets were exposed to the behavioral battery starting at stage

Conclusions

This study investigated the direct effects of constant light during early life (LL) on the development of psychological behavioral responding patterns in unfamiliar social contexts using human-reared marmosets. We implemented human care to remove potential entrainment from natural parent-rearing and to standardize developmental conditions. The LL group data was compared primarily to LD (the representative control group), with partial reference to an extreme condition (DD). The characterization

Acknowledgments

The authors thank Mr. P.C. Hart for his help with this MS, and Ms S. Foreman and Prof. P. Narins for their scientific advice. This work was supported by MEXT, Grant-in-Aid for Scientific Research on Innovative Areas (21200017), partially by JST, tsunagushikumi and A-step and MHLW, Intramural Research Grant 22-6 for Neurological and Psychiatric Disorders of NCNP.

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