Abstract
Sleep promotes memory consolidation in humans and many other species, but the physiological and anatomical relationships between sleep and memory remain unclear. Here, we show the dorsal paired medial (DPM) neurons, which are required for memory consolidation in Drosophila, are sleep-promoting inhibitory neurons. DPMs increase sleep via release of GABA onto wake-promoting mushroom body (MB) α'/β' neurons. Functional imaging demonstrates that DPM activation evokes robust increases in chloride in MB neurons, but is unable to cause detectable increases in calcium or cAMP. Downregulation of α'/β' GABAA and GABABR3 receptors results in sleep loss, suggesting these receptors are the sleep-relevant targets of DPM-mediated inhibition. Regulation of sleep by neurons necessary for consolidation suggests that these brain processes may be functionally interrelated via their shared anatomy. These findings have important implications for the mechanistic relationship between sleep and memory consolidation, arguing for a significant role of inhibitory neurotransmission in regulating these processes.
Highlights
Accumulating evidence suggests that sleep plays a role in promoting the consolidation of memory (Stickgold, 2005; Diekelmann and Born, 2010; Mednick et al, 2011; Abel et al, 2013; Rasch and Born, 2013)
To begin to probe these issues, we have investigated the role of the dorsal paired medial (DPM) neurons, which are critical to memory consolidation in Drosophila melanogaster, in the regulation of sleep
The anatomy involved in memory consolidation in mammals is highly complex and distributed, in the fly it is quite compact: the DPM neurons, a single pair of neurons innervating all of the mushroom body (MB) lobes, are the mediators of consolidation for odor memories (Waddell et al, 2000; Keene et al, 2004, 2006; Yu et al, 2005; Krashes and Waddell, 2008)
Summary
Accumulating evidence suggests that sleep plays a role in promoting the consolidation of memory (Stickgold, 2005; Diekelmann and Born, 2010; Mednick et al, 2011; Abel et al, 2013; Rasch and Born, 2013). Sleep deprivation following an associative learning task impairs consolidated memory in Drosophila, rodents, and humans whereas sleep immediately after a learning task improves consolidated memory across the same broad range of organisms (Ganguly-Fitzgerald et al, 2006; Donlea et al, 2011; Rasch and Born, 2013; Diekelmann, 2014). It is not, clear exactly how sleep promotes memory consolidation: it may be a permissive state generated by other brain regions that prevents sensory interference with memory circuits, or alternatively the memory circuitry itself may actively participate in sleep promotion as an integral aspect of the consolidation process. Critical memory information is transferred from short-term storage in neurons required for initial acquisition to anatomically and physiologically distinct long-term storage
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