Abstract
Virtually all animals have endogenous clock mechanisms that “entrain” to the light-dark (LD) cycle and synchronize psychophysiological functions to optimal times for exploring resources and avoiding dangers in the environment. Such circadian rhythms are vital to human mental health, but it is unknown whether circadian rhythms “entrained” to the LD cycle can be overridden by entrainment to daily recurring threats. We show that unsignaled nocturnal footshock caused rats living in an “ethological” apparatus to switch their natural foraging behavior from the dark to the light phase and that this switch was maintained as a free-running circadian rhythm upon removal of light cues and footshocks. Furthermore, this fear-entrained circadian behavior was dependent on an intact amygdala and suprachiasmatic nucleus. Thus, time-specific fear can act as a non-photic entraining stimulus for the circadian system, and limbic centers encoding aversive information are likely part of the circadian oscillator network that temporally organizes behavior.
Highlights
IntroductionMost animals exhibit rhythmic patterns of activity that are restricted to specific periods of the daily cycle, such as the daytime (diurnal), nighttime (nocturnal), or dawn-and-dusk times (crepuscular)[1,2,3]
Most animals exhibit rhythmic patterns of activity that are restricted to specific periods of the daily cycle, such as the daytime, nighttime, or dawn-and-dusk times[1,2,3]
Animals living in the closed economy chamber and maintained on a 12-h/12-h LD cycle quickly learned to press a lever to procure food pellets in the foraging area
Summary
Most animals exhibit rhythmic patterns of activity that are restricted to specific periods of the daily cycle, such as the daytime (diurnal), nighttime (nocturnal), or dawn-and-dusk times (crepuscular)[1,2,3] Such circadian rhythms are generated by endogenous molecular clocks that oscillate with approximately 24-h periods, but because these periods are usually slightly shorter or longer within individuals, these clocks must be “entrained” by external cues (zeitgebers or “time-givers”) to remain environmentally relevant[1,2,3,4,5]. In response to unsignaled nocturnal shock, animals switched their natural feeding and activity from the dark phase to the light phase This fear-induced diurnal behavior persisted (free-ran) when the light cues and footshocks were removed (Fig. 1c), and the phase of the free-running rhythm approximated the phase when the recurring threat was present, confirming that daily cyclic fear can act as a zeitgeber. The finding that amygala-coded fear can reprogram SCN-directed circadian behavior suggests that the amygdala is a part of the circadian oscillator network that temporally organizes behavior
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