Human Cortical Neurons in the Anterior Temporal Lobe Reinstate Spiking Activity during Verbal Memory Retrieval

Abstract

When we recall an experience, we rely upon the associations that we formed during the experience, such as those among objects, time, and place [1]. These associations are better remembered when they are familiar and draw upon generalized knowledge, suggesting that we use semantic memory in the service of episodic memory [2, 3]. Moreover, converging evidence suggests that episodic memory retrieval involves the reinstatement of neural activity that was present when we first experienced the event. Therefore, we hypothesized that retrieving associations should also reinstate the neural activity responsible for semantic processing. Indeed, previous studies have suggested that verbal memory retrieval leads to the reinstatement of activity across regions of the brain that include the distributed semantic processing network [4-6], but it is unknown whether and how individual neurons in the human cortex participate in the reinstatement of semantic representations. Recent advances using high-density microelectrode arrays (MEAs) have allowed clinicians to record from populations of neurons in the human cortex [7, 8]. Here we used MEAs to record neuronal spiking activity in the human middle temporal gyrus (MTG), a cortical region supporting the semantic representation of words [9-11], as participants performed a verbal paired-associates task. We provide novel evidence that population spiking activity in the MTG forms distinct representations of semantic concepts and that these representations are reinstated during the retrieval of those words.