Selective rapid eye movement sleep deprivation impairs the maintenance of long‐term potentiation in the rat hippocampus

Abstract

Rapid eye movement (REM) sleep deprivation (RSD) is known to impair learning and memory. Previous studies have demonstrated that RSD induces an impairment of hippocampal long-term potentiation (LTP). In most of these studies, RSD was set up prior to LTP induction. In this work, we focused on RSD after LTP induction. We investigated the effect of RSD for 24-48 h after induction of LTP in the dentate gyrus on LTP maintenance and whether a REM rebound after 48 h RSD affected LTP. RSD rats were deprived of REM sleep by stroking their backs using a brush, whereas control rats were allowed to sleep freely. Another control group of rats was awoken during non-REM sleep (NRS) under the same conditions (NRS group). REM-deprived rats displayed a faster decay of population spike amplitudes compared with the control and NRS groups over a 24-h recording time. After 48 h RSD, there was no difference in the population spike amplitudes before or after 4 h of release from RSD. These results suggest that REM sleep after LTP induction in the dentate gyrus plays an essential role in LTP maintenance, whereas a REM rebound does not restore the RSD-induced impairment of LTP.

The impact of sleep loss on hippocampal function

“…Researchers demonstrated that, similar to behavioral studies, LTP is vulnerable to total sleep deprivation, as well as to REM-specific sleep deprivation and fragmented sleep (McDermott et al 2003;Tartar et al 2006;Ravassard et al 2009;Florian et al 2011). Similar LTP deficits occurred after sleep deprivation in vivo in dentate gyrus-CA3 region (Romcy-Pereira and Pavlides 2004; Marks and Wayner 2005;Ishikawa et al 2006;Alhaider et al 2011). The in vivo studies demonstrated that this LTP deficit was not an artifact of slice preparation, but was a result of the influence of sleep deprivation on the intact hippocampal circuitry.…”

“…The in vivo studies demonstrated that this LTP deficit was not an artifact of slice preparation, but was a result of the influence of sleep deprivation on the intact hippocampal circuitry. The ability to induce LTP in vivo allowed researchers to investigate the effect of sleep deprivation on the maintenance phase of LTP, which exhibited impairment after total sleep deprivation and REM sleep deprivation in this paradigm (Romcy-Pereira and Pavlides 2004; Ishikawa et al 2006). This suggests that sleep deprivation perturbs molecular signaling pathways underlying both the induction phase and the maintenance phase of LTP.…”

The effects of rapid eye movement sleep deprivation and recovery on spatial reference memory of young rats

“…This phenomenon was considered to be a homeostatic compensation for a deficit in REM sleep (Ocampo-Garcés et al, 2000); however, the functional significance for memory is unclear. There is electrophysiological evidence that REM rebound does not restore the RSD-induced impairment of LTP (Ishikawa et al, 2006;Kim et al, 2005;Romcy-Pereira & Pavlides, 2004). For example, Ishikawa et al specifically examined the effect of RSD after LTP induction and REM rebound on LTP maintenance in DG; it was shown that a 24-to 48-h duration of RSD caused a significant decrease in population spike amplitudes and that REM rebound has no effect on RSD-induced impairment of LTP.…”

“…To our knowledge, there have been only three studies that have specifically examined whether REM rebound could restore the RSD-induced impairment of long-term potentiation (LTP; Ishikawa et al, 2006;Kim, Mahmoud, & Grover, 2005;Romcy-Pereira & Pavlides, 2004). A study on the effect of RSD for 24-48 h after induction of LTP in the dentate gyrus (DG) on LTP maintenance revealed that REM-deprived rats displayed a deficit in the maintenance of LTP and that the deficit continued to exist after 4 h of release from RSD (Ishikawa et al, 2006). Another study observed the impact of RSD for 4 h after LTP induction in DG and medial prefrontal cortex on the maintenance of LTP; it was shown that the impairment of the maintenance of LTP lasted for 48 h (Romcy-Pereira & Pavlides, 2004).…”

“…J. Silva, 2003). In recent years, evidence has been accumulating that consolidation of hippocampus-dependent memories relies on a dialogue between the neocortex and the hippocampus and that the crucial feature of this dialogue is the neuronal reactivation of newly formed memories during sleep (Born et al, 2006;Fu et al, 2007;Ishikawa and training day: The rats tended to more directly locate the platform on the training day before sleep deprivation. The 48-h REM sleep deprivation produced more circuitous swimming paths, and this delay in paths did not show significant improvement during sleep recovery.…”