Regulation of Hippocampal Firing by Network Oscillations during Sleep

Abstract

It has been hypothesized that waking leads to higher firing neurons, with increased energy expenditure, and sleep serves to return activity to baseline levels. Oscillatory activity patterns during different stages of sleep may play specific roles in this process, but consensus has been missing. To evaluate these phenomena in the hippocampus, we recorded from region CA1 neurons in rats across the 24-hr cycle and found that their firing increased upon waking, and decreased 11 % per hr across sleep. Waking and sleep also affected lower and higher firing neurons differently. Interestingly, the incidences of sleep spindles and sharp-wave ripples (SWRs), typically associated with cortical plasticity, were predictive of ensuing firing changes and more robustly than were other oscillatory events. Spindles and SWRs were initiated during non-REM sleep yet the changes were incorporated in the network over the following REM sleep epoch. These findings indicate an important role for spindles and SWRs and provide novel evidence of a symbiotic relationship between non-REM and REM stages of sleep in the homeostatic regulation of neuronal activity.

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

“…REMS and theta oscillations could play an important role in excitability homeostasis in the hippocampus. 69,70 The present data and our result showing a positive correlation between RM performance and the duration of rapid theta may indeed suggest a REMS homeostatic process needed to recalibrate cortical networks after the rule learning. This could limit an overflow of hippocampal networks and reset these networks for another RM task.…”

Sleep, synaptic homeostasis and neuronal firing rates

“…Using a set of > 1,000 putative CA1 pyramidal cells it found that wake bouts lasting > 15 min led to an increase in firing, while every hour of sleep led to a 11% decrease [16]. Specifically, across long (> 30 min) sleep episodes mean firing rates in NREM sleep declined during both the light and the dark period, and mean firing rates in REM sleep declined during the day (REM bouts at night were short and variable).…”

“…The decline in firing across NREM sleep correlated with the occurrence of sharp wave ripples (SWRs) and spindles (but not that of hippocampal slow wave activity), while the decline during REM sleep correlated with theta activity. Moreover, theta activity in REM sleep was positively correlated with the incidence rate of spindles and SWRs in the preceding NREM sleep episode, suggesting that the mechanisms underlying the sleep-dependent decline in firing were triggered in NREM sleep and fully actuated during REM sleep [16]. The authors divided the neurons in five quintiles based on their firing rate, and implemented a strict shuffle correction to account for regression to the mean.…”

“…The authors divided the neurons in five quintiles based on their firing rate, and implemented a strict shuffle correction to account for regression to the mean. They found that the decline in firing across sleep occurred in all CA1 neurons independent of their initial level of activity, but there were some differences: the slowest firing CA1 neurons showed the largest decline in firing across sleep, while moderately-firing neurons showed the largest increase in firing across wake [16]. The conclusion was that sleep has the same overall effect on all neurons – a decline in firing rate – but that the extent of these plastic changes differs, with low and medium firing cells showing the greatest firing “plasticity” across the sleep/wake cycle, and the fastest neurons being the least plastic [16,17].…”

“…They found that the decline in firing across sleep occurred in all CA1 neurons independent of their initial level of activity, but there were some differences: the slowest firing CA1 neurons showed the largest decline in firing across sleep, while moderately-firing neurons showed the largest increase in firing across wake [16]. The conclusion was that sleep has the same overall effect on all neurons – a decline in firing rate – but that the extent of these plastic changes differs, with low and medium firing cells showing the greatest firing “plasticity” across the sleep/wake cycle, and the fastest neurons being the least plastic [16,17]. Of note, another recent study found that relative to fast firing neurons, slow firing CA1 place cells promptly change their activity pattern in response to a novel environment, and show greater temporal coactivation and increased bursting during post-experience sleep [32].…”