SUPPRESSION OF LONG-TERM POTENTIATION INDUCTION DURING ALERT WAKEFULNESS BUT NOT DURING ENHANCED REM-SLEEP AFTER AVOIDANCE-LEARNING

Major learning events are typically followed by a period during which the number and/or duration of rapid-eye movement sleep episodes is inc reased. Processes critical to memory formation are thought to take pla ce during this interval of 'enhanced' rapid-eye movement sleep. We the refore compared the capacity for long-term potentiation during rapid-e ye movement sleep and alert wakefulness after learning. Rats were chro nically implanted with electrodes for stimulation of the perforant pat h and recording of evoked potentials and EEG in the dentate gyrus. Aft er obtaining baseline recordings, rats were trained on a 40-trial two- way active avoidance task. Conditioned rats exhibited a two-fold incre ase in the mean duration of rapid-eye movement sleep episodes, as refl ected by a prolongation of the hippocampal theta rhythm. There was no change in the sleep pattern of pseudoconditioned controls, which recei ved explicitly unpaired tones and foot shocks in a yoked design. High- frequency stimulation was applied during the second, third, and fourth major rapid-eye movement steep episodes after active avoidance traini ng. Another group was tetanized at matching time points during alert w akefulness. After pseudoconditioning, tetanus applied during wakefulne ss or rapid-eye movement sleep readily induced long-term potentiation, and there was no difference between groups in the magnitude of increa se for the population excitatory postsynaptic potential slope or the p opulation spike height as measured 1 h, 24 h, and 5 days post-tetanus. By contrast, in conditioned rats, tetanus applied during wakefulness failed to elicit long-term potentiation of the excitatory postsynaptic potential slope (7.6% increase 1h post-tetanus), while the group stim ulated during 'enhanced' rapid-eye movement sleep exhibited a 32% pote ntiation, equivalent to that obtained after pseudoconditioning. Analys is of individual experiments revealed a marked reduction in the probab ility of inducing long-term potentiation during post-learning wakefuln ess. We conclude that avoidance learning affects the induction of long -term potentiation in the dentate gyrus, suppressing induction during alert wakefulness while releasing the potential for synaptic modificat ion during episodes of rapid-eye movement sleep. The effect is compati ble with the hypothesis that memory consolidation involves a dynamic r egulation of events such as long-term potentiation during sleep and wa kefulness.