Human episodic memory retrieval is accompanied by a neural jump back in time

Cognitive psychologists have long hypothesized that experiences are encoded in a temporal context that changes gradually over time. When an episodic memory is retrieved, the state of context is recovered—a jump back in time. We recorded from single units in the MTL of epilepsy patients performing an item recognition task. The population vector changed gradually over minutes during presentation of the list. When a probe from the list was recollected, the population vector reset to the neighborhood of the original presentation of that probe during study—a neural “jump back in time.” Probes that were not recollected did not cause a jump back in time. These results constitute the first direct evidence that recollection of an episodic memory in humans is associated with recovery of a gradually-changing state of temporal context—a neural “jump-back-in-time” that parallels the act of remembering. Introduction Episodic memory refers to our ability to vividly remember specific events from our own experience. The vividness of episodic memory, along with the specificity of the memory to a particular place and time has led researchers to characterize episodic memory as mental time travel (Tulving, 1972; Hassabis et al., 2007; Schacter et al., 2007). This verbal description has been operationalized in computational models of episodic memory in which the flow of time is described by a slowly and gradually-changing state of temporal context (Howard and Kahana, 2002; Sederberg et al., 2008; Polyn et al., 2009; Howard et al., 2015). In these models episodic memory retrieval is accompanied by the recovery of a prior state of temporal context—a jump back in time—that accounts for the behavioral contiguity effect (Kahana, 1996; Schwartz et al., 2005; Howard et al., 2008; Unsworth, 2008). This computational hypothesis makes two predictions. First, in addition to stimulus-evoked activity, the activity of neurons involved in episodic memory should in addition also change gradually over time. This prediction aligns with a large body of animal work showing that neural ensembles in the hippocampus, amygdala and prefrontal cortex change slowly over time scales up to at least tens of minutes (Manns et al., 2007; Hyman et al., 2012; Mankin et al., 2012; MacDonald et al., 2011; Salz et al., 2016; Rubin et al., 2015; Cai et al., 2016; Rashid et al., 2016). Second, during retrieval of an existing memory, the prior state (temporal context) associated with an episodic memory should be restored. Although some prior studies have attempted to measure this hypothesized phenomenon (Manning et al., 2011; Howard et al., 2012; Yaffe et al., 2014), due to methodological limitations of those studies there is presently no definitive study linking this phenomenon to