Changes in dentate gyrus neuronal activity during sleep-wake cycle in mice

Abstract

Objective To investigate the difference of dentate gyrus (DG) neuronal activity between wakefulness and sleep state, and the characteristics of DG neuronal activity during hippocampal sharp wave ripple and θ oscillations. Methods Six 3-month-dd male wild-type C57BL/6 mice (22~25 g) were employed. The oscillation state of local field potential in the dorsal hippocampus and three-dimensional acceleration of the head and neck were used to determine the brain state which were classified into three types:wakefulness, non-rapid eye movement (NREM) sleep and rapid eye movement (REM) sleep. In vivo multi-electrode arrays were utilized to record the firing activity of DG neurons under distinct states. Results The DG neurons were divided into the granule cells, mossy cells and interneurons according to characteristics of spike rates and valley-to-peak spike waveform width. The firing rates of granule cells (n=75) in NREM sleep were significantly higher than those in either REM sleep (P < 0.05) or wakefulness (P < 0.05). The granule cells exhibited further elevated spike activity during sharp wave ripples during NREM sleep and θ oscillations during REM sleep (P < 0.05). The firing rates of mossy cells (n=27) in REM sleep were significantly higher than in either NREM sleep (P < 0.05) or wakefulness (P < 0.05), but no statistical difference was observed in firing rates between NREM sleep and wakefulness. Likewise, the mossy cells exhibited increased spike activity during sharp wave ripples in NREM sleep and θ oscillations in REM sleep (P < 0.05). The firing rates of interneurons (n=9) during REM sleep were significantly higher than that in NREM sleep (P < 0.05). However, there was no significant difference in spike activities of interneurons between NREM sleep and wakefulness. 67% of the DG interneurons increased their spike activities, whereas the remaining interneurons (33%) decreased their spike activities during sharp wave ripples. The spike activity of interneurons had greatest decline among 3 types of DG neurons (P < 0.05). Conclusion The granule cells and mossy cells in the DG area are significantly different between wakefulness and sleep states in the firing activities. The granule cells exhibit strongest firing activities during NREM sleep, whereas the mossy cells show strongest firing activities during REM sleep.

Keywords

• dentate gyrus
• hippocampus
• wakefulness
• sleep
• sharp wave ripple
• θ oscillation