Complex memories induced by intracranial electrical brain stimulation are related to complex networks

The precise and fleeting moment of rich recollection triggered by an environmental cue is difficult to reproduce in the lab. However, epilepsy patients can experience sudden reminiscences after intracranial electrical brain stimulation (EBS). In these cases, the transient brain state related to the activation of the engram and its conscious perception can be recorded using intracerebral EEG (iEEG). We collected various EBS-induced reminiscences for iEEG analysis, classifying them as follows: no or weak details (familiarity); moderate details and context (semantic and personal semantic memories); high details and context (episodic). Nine brain areas were selected within the temporal lobes (including the hippocampus and temporal neocortex, ipsi- and contralateral) and the insula, defining a network (each area as a node). Functional connectivity was measured by estimating pair-wise non-linear correlations between signals recorded from these brain regions during different memory events. Seventeen reminiscences in six patients (2 episodic, 10 personal semantic, 2 semantic memories, 5 familiar objects, 1 déjà-rêvé) were compared to 18 control experiential phenomena (unrelated to reminiscence), 18 negative EBS (which failed to elicit memories or other phenomena) in the same locations, and pre-EBS baseline activity. The global functional connectivity in the network was higher following EBS-induced reminiscences than during baseline activity, control phenomena, or negative EBS. The degree of connectivity increased with the complexity of memories; it was higher for detailed and contextualized memories like episodic memories. More significant links compared to baseline (edges with higher non-linear correlation relative to baseline) were observed for episodic memories than for less contextualized memories. These increases in connectivity occurred in all frequency bands, except the delta band. Our results support understanding declarative memory retrieval as having a multiplexed organization. They also show that richer memories activated by intracranial EBS are related to more complex connectivity patterns across medial and neocortical temporal lobe structures.