Decoding individual episodic memory traces in the human hippocampus

Abstract

In recent years, multivariate pattern analyses have been performed on functional magnetic resonance imaging (fMRI) data, permitting prediction of mental states from local patterns of blood oxygen-level-dependent (BOLD) signal across voxels. We previously demonstrated that it is possible to predict the position of individuals in a virtual-reality environment from the pattern of activity across voxels in the hippocampus. Although this shows that spatial memories can be decoded, substantially more challenging, and arguably only possible to investigate in humans, is whether it is feasible to predict which complex everyday experience, or episodic memory, a person is recalling. Here we document for the first time that traces of individual rich episodic memories are detectable and distinguishable solely from the pattern of fMRI BOLD signals across voxels in the human hippocampus. In so doing, we uncovered a possible functional topography in the hippocampus, with preferential episodic processing by some hippocampal regions over others. Moreover, our results imply that the neuronal traces of episodic memories are stable (and thus predictable) even over many re-activations. Finally, our data provide further evidence for functional differentiation within the medial temporal lobe, in that we show the hippocampus contains significantly more episodic information than adjacent structures.

Figure 1

Experimental Protocol (A) Still photographs taken from one of the film clips viewed during prescan training. The clip depicts a woman taking a drink from a disposable coffee cup and then putting it in a rubbish bin (trash can). (B) Timeline of a single trial during fMRI scanning. For details, see Supplemental Experimental Procedures.

Figure 2

Mean Decoding Accuracy Results with Standard Errors for the Hippocampus, Entorhinal Cortex, and Parahippocampal Gyrus Proportion accuracy values are shown on the vertical axis; the dashed line at 0.33 represents chance-level performance. All three areas were significantly above chance-level performance, with hippocampus (HC) accuracy significantly greater than both entorhinal cortex (EC) and parahippocampal gyrus (PHG) (one-way analysis of variance, p = 0.027; post hoc t tests: HC > EC, p = 0.035; HC > PHG, p = 0.048; no significant difference between EC and PHG, p = 0.86). See Supplemental Experimental Procedures and Figure S1 for more details. Error bars represent the standard error of the mean.

Figure 3

Individual Participant Data Hippocampal information maps in the left and right hippocampi are shown for the ten participants (P1–P10) on zoomed-in sagittal sections of the medial temporal lobes taken from each participant's structural MRI scan. Each map represents the set of voxels carrying the most episodic information within the hippocampus. See Supplemental Experimental Procedures and Figure S2 for more details.

Figure 4

Consistency of Results across Participants Frequency heat maps for the left and right hippocampi shown on zoomed-in sagittal sections from one of the participant's structural MRI scans chosen at random. Frequency scale is shown at the left. To determine statistical significance, we compared the frequency value at each voxel against the binomial distribution, and the peak regions in yellow and red all survived an uncorrected p < 0.001 level of significance.