Circadian rhythms in humans and animals are sensitive to stressors and changes in the emotional state. However, whether circadian rhythms can be entrained by fear stimuli had not been directly investigated until now. To test this, circadian behaviors of male Long Evan rats maintained on an LD (12-h light/12-h dark) cycle were monitored in a live-in chamber comprised of safe nesting and risky foraging areas. Initially, animals pressed a lever to procure food pellets in the foraging area and were entrained to the environmental conditions for a week.
Then, animals were subjected to (i) 14 days of ‘Unsignaled’ footshocks (0.8 mA; pseudo-random 2 shocks/hr) which were delivered only during the dark phase of the LD cycle, and (ii) 14 days of ‘Signaled’ footshocks (a 9-sec light cue preceding the footshock) also during the dark cycle (counterbalanced orders). During the unsignaled footshock, rats reversed their normal circadian feeding behavior, meaning that they exhibited more feeding behavior during the light phase than the dark phase, and showed arrhythmic locomotor activity. During the signaled footshock, however, rats returned to or conserved their normal circadian feeding (i.e., the feeding behavior was observed mostly during the dark phase) and rhythmic locomotor activity. In sum, rats exposed the unpredictable stressor (i.e. unsignaled shock) quickly learned to adapt their behavior by shifting their meal time earlier so that there was a lesser possibility of the feeding coinciding with the shock. Furthermore, lesioning the amygdala in these animals prevented the reversal of the feeding time, suggesting that amygdala function is causal in producing this effect and postulating a new role for amygdala function.
These results suggest that amygdala-dependent fear, associated with environmental threats limited to the naturally active phase (i.e. dark), can act as a non-photic entraining stimulus and lead to circadian activity during the naturally inactive phase (i.e. light). Importantly, there is growing evidence suggesting a link between mood disorders such as depression and anxiety and disturbances in circadian rhythm, which makes determining the mechanism underlying the entrainment of circadian rhythm by fearful or stressful stimuli of clinical relevance. Moreover, if aversive conditioning is able to induce changes in circadian rhythm, can appetitive conditioning do the same?
E.E. S. Kim, J. Kashima, O. Motch, H.O. de la Iglesia, J.J. Kim. Entrainment of circadian rhythms by fear. Program No. 189.04/HHH29.2013. Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2013.