Memory for Time of Day (Time Memory) Is Encoded by a Circadian Oscillator and Is Distinct From Other Context Memories

Abstract

We report that the neural representation of the time of day (time memory) in golden hamsters involves the setting of a 24-h oscillator that is functionally and anatomically distinct from the circadian clock in the suprachiasmatic nucleus (SCN), but is entrained by the SCN acting as a weak zeitgeber. In hamsters, peak conditioned place avoidance (CPA) was expressed only near the time of day of the learning experience (±2 h) for the first days after conditioning. On a 14:10 light:dark cycle, with conditioning at the end of the light period (zeitgeber time 11 [ZT11]), CPA behavior, including time of day memory, was retained for more than 18 d. With conditioning in the early day (zeitgeber time 03 [ZT03]), CPA was completely lost after 5 d but reemerged after an additional 6 d, with the peak avoidance time shifted to ZT11. When the entraining light cycle was shifted immediately following learning at either ZT11 or ZT03, with no additional experience in the training apparatus, peak CPA 18 d later was always found at ZT11 on the shifted light cycles. When conditioned at ZT03, then placed into constant dark for 18 cycles, the peak shifted to subjective circadian time 11 (CT11). In all experiments, the peak CPA time was set initially to the time of experience, and was reset subsequently to the end of the subjective day, without memory loss for other context associations. In the absence of an SCN, peak avoidance was not reset. Therefore, time memory is distinct from other context memories, and involves the setting of a non-SCN circadian oscillator. We suggest that circadian oscillators underlying time memory work in concert with the SCN to enable anticipation of critical conditions according to both immediate- and long-term probabilities of where and when important conditions could be encountered again. (Author correspondence: [email protected])

Keywords:

• Conditioning
• Learning
• Place avoidance
• Place preference
• Rhythm

ACKNOWLEDGMENTS

The authors wish to thank Dr. Nicholas Mrosovsky for recommendations on an earlier version of the manuscript. The authors would like to thank the numerous undergraduate students at the University of Toronto who made contributions to the work, with special thanks to Seung Cheol Kim, Ricardo Baltazar, and Michael Siu.

Declaration of Interest: The work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grant number 170040) to M.R.R.

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.