Sequential replay of nonspatial task states in the human hippocampus

Abstract

Sequential neural activity patterns related to spatial experiences are “replayed” in the hippocampus of rodents during rest. We investigated whether replay of nonspatial sequences can be detected noninvasively in the human hippocampus. Participants underwent functional magnetic resonance imaging (fMRI) while resting after performing a decision-making task with sequential structure. Hippocampal fMRI patterns recorded at rest reflected sequentiality of previously experienced task states, with consecutive patterns corresponding to nearby states. Hippocampal sequentiality correlated with the fidelity of task representations recorded in the orbitofrontal cortex during decision-making, which were themselves related to better task performance. Our findings suggest that hippocampal replay may be important for building representations of complex, abstract tasks elsewhere in the brain and establish feasibility of investigating fast replay signals with fMRI.

Hippocampal ensembles represent sequential relationships among discrete nonspatial events

“…For instance, it is well established that neural activity in regions associated with planning behavior, including the prefrontal cortex and striatum, is significantly entrained to the hippocampal theta rhythm [34][35][36] . This proposal is consistent with recent work using this and other temporal memory tasks showing that, in addition to the hippocampus, the prefrontal cortex is also strongly engaged during task performance in both rodents and humans 23,24,[37][38][39][40] . However, the specific prefrontal mechanisms remain to be demonstrated.…”

Episodic memory retrieval success is associated with rapid replay of episode content

“…For reverse replay events (in the after condition), and for forward replay events (in the before condition), this analysis localized activity at replay onset to the right anterior MTL, encompassing the hippocampus and entorhinal cortex (after: z = 3.72, p <0.001 whole-brain FWE; before: z = 3.73, p < 0.001 whole-brain FWE; Fig. 4a, c; Table S2), consistent with human fMRI results during rest in a cognitive paradigm (30). The increase in MTL power was selective to replay onset ( Fig.…”

“…Participants were recruited from the UCL Institute of Cognitive Neuroscience Subject Database. Data from three participants were excluded due to poor memory performance (described below) leaving data from 25 participants for analyses (14 female; mean age 24 (range[18][19][20][21][22][23][24][25][26][27][28][29][30][31][32]. Participants were required to meet the following criteria: age between 18-35, fluent English speaker, normal or correctedto-normal vision, without current neurological or psychiatric disorders, no nonremovable metal, and no participation in an MRI scan in the two days preceding the MEG session.…”

Synaptic learning rules for sequence learning

“…Consequently, the behavioral sequence could be replayed (as illustrated e.g. by simulations in 17) and the memory of the temporal order of events is recalled (18,19).…”