Content Tuning in the Medial Temporal Lobe Cortex: Voxels that Perceive, Retrieve

Abstract

How do we recall vivid details from our past based only on sparse cues? Research suggests that the phenomenological reinstatement of past experiences is accompanied by neural reinstatement of the original percept. This process critically depends on the medial temporal lobe (MTL). Within the MTL, perirhinal cortex (PRC) and parahippocampal cortex (PHC) are thought to support encoding and recall of objects and scenes, respectively, with the hippocampus (HC) serving as a content-independent hub. If the fidelity of recall indeed arises from neural reinstatement of perceptual activity, then successful recall should preferentially draw upon those neural populations within content-sensitive MTL cortex that are tuned to the same content during perception. We tested this hypothesis by having eighteen human participants undergo functional MRI (fMRI) while they encoded and recalled objects and scenes paired with words. Critically, recall was cued with the words only. While HC distinguished successful from unsuccessful recall of both objects and scenes, PRC and PHC were preferentially engaged during successful versus unsuccessful object and scene recall, respectively. Importantly, within PRC and PHC, this content-sensitive recall was predicted by content tuning during perception: Across PRC voxels, we observed a positive relationship between object tuning during perception and successful object recall, while across PHC voxels, we observed a positive relationship between scene tuning during perception and successful scene recall. Our results thus highlight content-based roles of MTL cortical regions for episodic memory and reveal a direct mapping between content-specific tuning during perception and successful recall.

Keywords: episodic memory; fMRI; hippocampus; medial temporal lobe; parahippocampal cortex; perirhinal cortex.

Figure 1.

Experimental paradigm. A, The fMRI task consisted of two object and two scene runs, each comprising an encoding and a retrieval phase. During encoding, participants saw adjective-object or adjective-scene pairs. During retrieval, only the adjective was presented, and participants tried to recall the associated object or scene from memory. Not shown: each fMRI trial was followed by 10 s of an active baseline task (inter-trial interval, ITI, arrows task), and the encoding phase was preceded and followed by a resting phase (odd-even numbers task, 180 s; see main text for details). B, In the post-fMRI recall task, participants typed in descriptions of the associated object and scene for each adjective.

Figure 2.

MTL ROIs and univariate retrieval results. A, To illustrate ROI localization, manually delineated ROIs for each participant’s HC, PRC, and PHC were MNI normalized, averaged across participants, and projected on the mean normalized T1 (averaged ROI threshold > 0.5). B–D, Retrieval-phase β values were averaged within each participant’s individual ROIs and submitted to group analyses. HC (B) showed a main effect of successful recall, while PRC (C) and PHC (D) additionally showed interaction effects, indicating preference for object recall (PRC) and scene recall (PHC), respectively. O: object, S: scene, R: recalled, F: forgotten. Error bars denote SEM; *p < 0.05 (two-tailed) for pairwise t tests.

Figure 3.

PRO. A, Illustrative data from two single participants’ ROIs; t values from the objects > scenes perception contrast (x-axes, positive voxels only) are plotted against t values from the object recall contrast (PRO-O, left column), while t values from the scenes > objects perception contrast (positive voxels only) are plotted against the scene recall contrast (PRO-S, right column). Data points indicate single voxels. In these example data, PRC voxels with greater effect sizes for object perception tended to show greater effect sizes for successful object recall (upper left scatterplot). Similarly, PHC voxels with greater effect sizes for scene perception tended to show greater effect sizes for successful scene recall (lower right scatterplot). Note that these within-participant scatterplots are for visualization only. B, Group averages of Fisher z-transformed correlation coefficients for PRO-O and PRO-S for PRC and PHC. Across PRC voxels, object tuning predicted object recall (PRO-O), but scene tuning did not predict scene recall (PRO-S). Across PHC voxels, scene tuning predicted scene recall, but object tuning did not predict object recall; *p < 0.05, (*)p < 0.1 (two-tailed) for one-sample and paired t tests, n.s.: not significant. Error bars denote SEM.