Lack of circadian entrainment and limited nocturnal plasticity in response to a cyclic aversive stimulus in a diurnal rodent, the antelope ground squirrel (Ammospermophilus leucurus)

Abstract

Recent studies have shown that cyclic aversive stimuli, such as random footshocks, act as a nonphotic zeitgeber to entrain circadian behaviors in nocturnal rodents, a pattern termed "fear entrainment". However, it remains unknown whether diurnal species exhibit similar plasticity in behavioral timing. This study aimed to determine if antelope ground squirrels (Ammospermophilus leucurus; AGS), a naturally diurnal rodent, can also shift their activity patterns to cyclic aversive stimuli. We conducted two experiments with 20 AGS housed in custom cages featuring a safe nesting area and a separate foraging area (for feeding and drinking), rendered aversive by presentation of unsignaled, time-specific footshocks. In the first experiment, animals were subjected to a 12:12 light-dark (LD) cycle. One group experienced aversion during the light phase, while the control group received the same treatment during the dark phase. In the second experiment, a 16:8 LD cycle was used, and animals were divided into three groups with the foraging area rendered aversive either during the first or second half of the light phase or during the dark phase. Following each of these treatments, animals were released into constant darkness (DD) to assess the phase and period of free-running rhythms. Contrary to previous findings in nocturnal rodents, AGS did not exhibit consistent shifts in activity to avoid footshocks. Most animals maintained their normal diurnal activity, with only minor and inconsistent phase shifts. In experiment two, animals exposed to footshocks during half of the light phase also failed to reliably shift activity to the opposite "safe" portion of the light phase. Together, these findings show AGS lack the ability to entrain to cyclic aversive stimuli or become nocturnal; this result suggests a lack of substantial plasticity in activity timing. These results highlight the importance of considering species-specific differences in nonphotic circadian entrainment and temporal niche plasticity.