Abstract

This study examined whether theta oscillations were compromised by the type of circadian disruption that impairs hippocampal-dependent memory processes. In prior studies on Siberian hamsters, we developed a one-time light treatment that eliminated circadian timing in the central pacemaker, the suprachiasmatic nucleus (SCN). These arrhythmic animals had impaired hippocampal-dependent memory whereas animals made arrhythmic with SCN lesions did not. The current study examined whether theta oscillations are compromised by the same light treatment that produced memory impairments in these animals. We found that both methods of inducing circadian-arrhythmia shortened theta episodes in the EEG by nearly 50%. SCN-lesioned animals, however, exhibited a 3-fold increase in the number of theta episodes and more than doubled the total time that theta dominated the EEG compared to SCN-intact circadian-arrhythmic animals. Video tracking showed that changes in theta were paralleled by similar changes in exploration behavior. These results suggest that the circadian-arrhythmic SCN interferes with hippocampal memory encoding by fragmenting theta oscillations. SCN-lesioned animals can, however, compensate for the shortened theta episodes by increasing their frequency. Implications for rhythm coherence and theta sequence models of memory formation are discussed.

Highlights

  • Theta oscillations are critical for memory processing

  • Given the importance of hippocampal theta oscillations in memory encoding, we investigated the impact of suprachiasmatic nucleus (SCN) arrhythmia on those oscillations to see if disruptive phase shift (DPS) hamsters exhibited changes in theta that might account for their memory deficits

  • Once these animals were made circadian-arrhythmic by the DPS protocol, bouts of activity occurred throughout the day and night (Figure 2A)

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Summary

Introduction

Theta oscillations are critical for memory processing. They arise from the coordinated firing patterns of neuronal ensembles within brain structures and across brain regions. Theta rhythms in the rodent electroencephalogram (EEG) oscillate at a frequency typically between 5–12 Hz, but the exact frequency is influenced by several factors such as species [2], time of day [3], sleep state [4], and brain temperature [5]. These oscillations dominate EEG signals during activities that support working memory and the encoding of episodic memories, such as when animals explore novel objects or navigate their environment [1,6]. Optogenetic disruption of theta rhythms during development in rats produced spatial memory deficits that persisted into adulthood [7], and in humans, enhancement of theta oscillations by brief localized magnetic stimulation improved visual working memory capacity in healthy adult subjects [8]

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