Human episodic memory retrieval is accompanied by a neural contiguity effect

Abstract

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 remembered with high confidence, the population vector reinstated the temporal context of the original presentation of that probe during study-a neural contiguity effect that provides a possible mechanism for behavioral contiguity effects. This pattern was only observed for well-remembered probes; old probes that were not well-remembered showed an anti-contiguity effect. These results constitute the first direct evidence that recovery of an episodic memory in humans is associated with retrieval of a gradually-changing state of temporal context-a neural "jump-back-in-time" that parallels the act of remembering. Significance statement. Episodic memory is the ability to re-live a specific experience from one's life. For decades, researchers have hypothesized that, unlike other forms of memory that can be described as simple associations between stimuli, episodic memory depends on the recovery of a neural representation of spatiotemporal context. During study of a sequence of stimuli, the brain state of epilepsy patients changed slowly over at least a minute. When the participant remembered a particular event from the list, this gradually-changing state was recovered. This provides direct confirmation of the prediction from computational models of episodic memory. The resolution of this point means that the study of episodic memory can focus on the mechanisms by which this representation of spatiotemporal context is maintained and, sometimes recovered.

Structuring Time in Human Lateral Entorhinal Cortex

“…This might explain the observed pattern similarity structure with relatively increased similarity for objects encountered in temporal proximity during learning and decreased similarity for items encountered after longer delays. While this interpretation is in line with data from rodent electrophysiology (Tsao et al, 2018) and the framework proposed by the temporal context model (Howard and Kahana, 2002;Howard et al, 2005) as well as evidence for neural contiguity effects in image recognition tasks (Howard et al, 2012;Folkerts et al, 2018), we cannot test the reinstatement of specific activity patterns from the learning phase directly since fMRI data were only collected during the picture viewing tasks in this study.…”

“…Changes in metabolic states and arousal presumably varied more linearly over time. Slowly drifting activity patterns have been observed also in the human medial temporal lobe (Folkerts et al, 2018) and EC specifically (Lositsky et al, 2016). A representation of time within a known trajectory in the alEC could underlie the encoding of temporal relationships between events in our task, where participants repeatedly navigated along the route to learn the positions of objects.…”

Time cells in the human hippocampus and entorhinal cortex support episodic memory

“…The activity of time cells in the mesial temporal lobe may provide a mechanism for the coding of temporal information that is necessary for the formation of these memories (1)(2)(3)(4)(5)(6). The spiking of these cells reliably increases at specific 25 moments within a fixed interval, with different groups of cells tuned to represent distinct but overlapping moments. The detailed temporal information available from a population of these time cells allows the hippocampus to impose temporal order on representations of individual items.…”

Overlap between hippocampal pre‐encoding and encoding patterns supports episodic memory

“…The Temporal Context Effect refers to the increased probability of sequentially recalling two items that were studied in close temporal contiguity (Polyn & Kahana, 2008;. This effect is supported by the hippocampus and its adjacent structures (Folkerts et al, 2018;Kragel et al, 2015;Manning et al, 2011) and is thought to arise from the largely overlapping temporal (and neural) contexts shared by neighboring items. That the magnitude of the Temporal Context Effect is predicted by pre-encoding/ encoding overlap further establishes the importance of the neurocognitive context prior to learning to successful encoding.…”

“…The effect is thought to arise from the largely overlapping temporal contexts shared by neighboring items and is a hallmark of episodic recall (Healey, 2018;Healey & Kahana, 2014;Healey, Long, & Kahana, 2018;Polyn et al, 2009). On the neural level, both memory allocation and the Temporal Context Effect have been shown to be associated with the hippocampus and adjacent structures (Folkerts, Rutishauser, & Howard, 2018;Josselyn & Frankland, 2018;Kragel, Morton, & Polyn, 2015;Manning et al, 2011;Rogerson et al, 2014). On the cognitive level, the extent of pre-encoding/encoding overlap reflects the similarity between the neurocognitive context before and during learning, with more similar contexts entailing greater likelihood of relying on contextual cues to drive memory.…”