Abstract

Emotional events are often better remembered than neutral events, and this benefit depends on the amygdala. We have previously demonstrated that brief basolateral amygdala electrical stimulation enhances memory in rodents. This study examined whether human amygdala stimulation immediately following the presentation of neutral object photographs enhanced later recognition memory following a night of sleep. We recruited 14 epilepsy patients undergoing intracranial EEG (iEEG) with depth electrode contacts placed in basolateral amygdala and sub-regions of the hippocampus. During continuous iEEG, each participant was presented a series of photographs of neutral objects, half of which were followed immediately by a unilateral stimulation to the amygdala (8 trains of 50-Hz pulses for 1-second at 0.5 mA after image offset). No epileptiform activity was elicited by the stimulation. Participants reported no awareness of the stimulation. Recognition memory and subjective confidence for half the photographs was tested immediately after the study session and for the other half of the photographs after a night of sleep. On the recognition memory test administered the following day, participants recognized neutral objects initially followed by amygdala stimulation more accurately than control objects. The result was similar when only high-confidence judgments were included. On the immediate recognition memory test without intervening sleep, participants performed similarly for both object conditions. We are also currently investigating how duration and quality of intervening sleep related to subsequent memory performance and network oscillatory activity. Similar to the prior rodent studies, the current results indicate that direct electrical stimulation to the human amygdala can enhance item-specific memory for neutral stimuli in the absence of awareness of the stimulation, and following a night of sleep, reflecting a key role of the amygdala in prioritizing experiences for long-term storage in declarative memory. Amygdala stimulation likely engages amygdala-hippocampus connections that normally serve to prioritize memory for emotional events and may provide a therapeutic route for patients with memory deficits Sleep Research Society Foundation support to JTW. Defense Advanced Research Projects Agency support to JTW, CSI, and REG.

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