Progress in Neuro-Psychopharmacology and Biological Psychiatry
Effects of constant daylight exposure during early development on marmoset psychosocial behavior
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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