Similarity breeds proximity: pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity

Abstract

Experiences unfold over time, but little is known about the mechanisms that support the formation of coherent episodic memories for temporally extended events. Recent work in animals has provided evidence for signals in hippocampus that could link events across temporal gaps; however, it is unknown whether and how such signals might be related to later memory for temporal information in humans. We measured patterns of fMRI BOLD activity as people encoded items that were separated in time and manipulated the presence of shared or distinct context across items. We found that hippocampal pattern similarity in the BOLD response across trials predicted later temporal memory decisions when context changed. By contrast, pattern similarity in lateral occipital cortex was related to memory only when context remained stable. These data provide evidence in humans that representational stability in hippocampus across time may be a mechanism for temporal memory organization.

Figure 1. Experimental Design

(A) Participants performed an associative encoding task on each trial. Scene stimuli repeated across either 2 or 4 consecutive trials, while object and face stimuli were trial unique. Objects and faces that were separated by a change in the associated scene made up the context boundary condition, while objects and faces that were paired with the same scene made up the same context condition. (B) Following each encoding block, participants performed a memory test in which they were asked to rate the temporal proximity of pairs of items from the encoding block. Participants made their responses on a 4-point scale: very close, close, far, very far. For the purposes of the behavioral and fMRI analyses, responses were collapsed into two bins: close and far. Temporal memory was analyzed based on whether the item pairs were from the context boundary or same context conditions during encoding. (C) Following the scan session, participants performed a surprise source memory test for the associations between the trial-unique faces and objects, and their paired scene stimuli. Participants were presented on each trial with a face or object from encoding and two alternatives for the associated scene stimulus. Participants chose either the left or right scene stimulus while indicating high or low confidence.

Figure 2. Behavioral Results

(A) Mean proportion of pairs that participants labeled close compared to far. Participants were more likely to rate same context pairs as close compared to context boundary pairs. Within the same context condition, participants were also more likely to rate pairs as close compared to far. (B) Mean response times to label pairs as close and far. For pairs labeled close, participants were slower to label context boundary pairs compared to same context pairs. Error bars denote standard error of the mean.

Figure 3. Encoding Pattern Similarity in Hippocampus and LO is Associated with Temporal Memory

(A) Pattern similarity for pairs of items labeled close was higher than for pairs labeled far in left hippocampus. (B) Left hippocampal pattern similarity was enhanced for close pairs relative to far pairs in the context boundary condition. See also Figure S1 and Table S1. (C) Pattern similarity was also enhanced for close pairs compared to far pairs in left LO. (D) In contrast to left hippocampus, pattern similarity in left LO differentially predicted close/far memory in the same context condition, leading to a region X context condition X memory response interaction (p < .03). Error bars denote standard error of the mean (see also Figure S2).

Figure 4. Pattern Similarity Searchlight Analysis

(A) A whole-brain searchlight analysis revealed a number of regions such as right intraparietal sulcus (pictured) in which pattern similarity was enhanced for context boundary pairs compared to same context pairs (p < .05 corrected). (B) The searchlight analysis also identified regions such as right medial prefrontal cortex (pictured) in which pattern similarity was enhanced for same context pairs relative to context boundary pairs. Critically, the searchlight analysis identified no regions in which overall pattern similarity was related to later temporal memory (p < .05 corrected). Error bars denote standard error of the mean (see also Table S2).