HUNGER AND SLEEP UTILIZE DIFFERENT BRAIN SYSTEMS FOR FORMING SPATIAL MEMORY

The slow consolidation of newly encoded memory is known to utilize sleep driving long-term memory formation in a hippocampus-dependent active systems consolidation process. However, evidence suggests that long-term memory can be formed also in the wake state when the animal is starving. Here, we show in rats that hunger consolidates spatial long-term memory that, unlike sleep-dependent consolidation, does not rely on hippocampal traces. After a 24-hour food deprivation period, rats encoded object locations on a standard object-place recognition (OPR) task with encoding followed by a 2-consolidation interval, during which the rats either received food and slept (Sleep-Full) or were awake (Wake-Full), or remained hungry and were awake (Wake-Hunger). At a retrieval test 24 hours later, the Wake-Hunger rats, like the Sleep-Full rats, exhibited full-blown object-place memory, whereas Wake-Full rats failed to show any memory. Hunger-consolidated memory was abolished after blocking neuropeptide-Y (NPY) signaling during the 2-hour consolidation phase. Inhibiting pharmacologically hippocampal function during the retrieval or consolidation phase, respectively, nullified expression of object-place memory after sleep-consolidation but left intact the memory consolidated in the hungry condition. Optogenetic hippocampal suppression during encoding, likewise, specifically spared hunger-dependent consolidation. Conversely, pharmacological inhibition of retrosplenial cortex during retrieval abolished spatial memory consolidated during hunger but not sleep-consolidated memory. The findings provide first-time evidence that the brain uses different systems and representations for forming spatial long-term memory dependent on the brain-state: i.e., sleep versus hunger.