Episodic memory consolidation by reactivation of human concept neurons during sleep reflects contents, not sequence of events

Abstract

How do our brains manage to store our everyday experiences into memory? Neurons in the human temporal lobe that respond to the concept of an individual person or object have been shown to provide the semantic building blocks for episodic memory. Recording from 1433 neurons in neurosurgical patients who learned a story involving specific concepts, we found reactivation of neurons representing these concepts during slow-wave sleep after learning. Concept neurons were conjointly reactivated, particularly during sharp-wave ripples, with time lags suitable for synaptic modification. However, the temporal sequence of reactivation did not reflect the sequence of concepts in the learned story. Unlike rodent place cells, which can acquire preferred firing locations during exploration of new environments according to their pre-existing preferred sequence of activation, human concept neurons are tuned to specific semantic contents before learning starts. Consequently, pre-existing firing sequences correlate with consecutive place fields in rodents, but not with sequences of events in human experience. Thus, in contrast to reactivation of rodent place cells, reactivation of human concept cells does not reflect sequences of events in human experience.