Shifting Gears in Hippocampus: Temporal Dissociation between Familiarity and Novelty Signatures in a Single Event

Abstract

The hippocampus is known to be involved in encoding and retrieval of episodes. However, real-life experiences are expected to involve both encoding and retrieval, and it is unclear how the human hippocampus subserves both functions in the course of a single event. We presented participants with brief movie clips multiple times and examined the effect of familiarity on the hippocampal response at event onset versus event offset. Increased familiarity resulted in a decreased offset response, indicating that the offset response is a noveltyrelated signature. The magnitude of this offset response was correlated, across hippocampal voxels, with an independent measure of successful encoding, based on nonrepeated clips. This suggests that the attenuated offset response to familiar clips reflects reduced encoding. In addition, the posterior hippocampus exhibited an increased onset response to familiar events, switching from an online familiarity signal to an offline novelty signal during a single event. Moreover, participants with stronger memory exhibited increased reactivation of online activity during familiar events, in line with a retrieval signature. Our results reveal a spatiotemporal dissociation between novelty/encoding and familiarity/retrieval signatures, assumed to reflect different computational modes, in response to the same stimulus.

The Consolidation and Transformation of Memory

“…When using multiple repetitions to gradually increase clip familiarity, the hippocampal offset response was attenuated, in line with an encoding signal. Conversely, the onset response increased with familiarity, suggesting the online hippocampal response primarily reflects retrieval, rather than encoding (Ben-Yakov et al, 2014).…”

Constructing Experience: Event Models from Perception to Action

“…One possibility is that the within-event binding function of the HPC (in collaboration with other brain systems) and its episodic memory formation function are complementary, reflecting distinct components of the cascade that occurs at an event boundary. Ben-Yakov and colleagues [108–110] have proposed that phasic activity in the HPC at the ends of events implements a “now print” function, compiling accumulated bound event representations in a way that enables their retrieval after a delay. They found that univariate activity in the HPC was time-locked to the ends of movie clips, and that the magnitude of this activity predicted the likelihood of remembering the just-ended clip (see also [111].…”

“…During an ongoing event, the HPC may bind disparate concurrently-activated cortical representations into a coherent complex. At an event boundary, the HPC may perform a “now print” function [108–110] or “sharpening” function [105] that stabilized the bound pattern in a way that preserves it for subsequent recall, before abandoning the current binding to make room for binding a new working model (see Figure 4).…”

Memory Retrieval in Mice and Men

“…Such conditions may result in generalization/inference (Moses et al 2006;Shohamy and Wagner 2008;Kumaran and McClelland 2012), interfer-ence (Müller and Pilzecker 1900;Anderson 2003;Wixted 2004), or creation of false memories Loftus 2005). Increasingly sensitive analyses methods of human brain imaging provide improved abilities to probe the interactions between encoding of new information and reactivation of previous representations (Staresina et al 2012b;Ben-Yakov et al 2014;Brown et al 2015).…”