Content-specific source encoding in the human medial temporal lobe

Abstract

Although the medial temporal lobe (MTL) is known to be essential for episodic encoding, the contributions of individual MTL subregions remain unclear. Data from recognition memory studies have provided evidence that the hippocampus supports relational encoding important for later episodic recollection, whereas the perirhinal cortex has been linked with encoding that supports later item familiarity. However, extant data also strongly implicate the perirhinal cortex in object processing and encoding, suggesting that perirhinal processes may contribute to later episodic recollection of object source details. To investigate this possibility, encoding activation in MTL subregions was analyzed on the basis of subsequent memory outcome while participants processed novel scenes paired with 1 of 6 repeating objects. Specifically, encoding activation correlating with later successful scene recognition memory was evaluated against that of source recollection for the object paired with the scene during encoding. In contrast to studies reporting a link between perirhinal cortex and item familiarity, it was found that encoding activation in the right perirhinal cortex correlates with successful recollection of the paired object. Furthermore, other MTL subregions also exhibited content-specific source encoding patterns of activation, suggesting that MTL subsequent memory effects are sensitive to stimulus category.

Figure 1

Schematic of a single encoding trial. A full-color, trial-unique scene is presented in the center of the screen with one of six objects, here a cup, presented in the upper left corner of the scene image. This composite image is presented for 4750 ms. Participants are instructed to imagine using the object in the scene during this time. After a 250 ms pause, a response screen with a green fixation cross appears for 1000 ms. During this time, participants are instructed to indicate whether or not they were successful at the encoding task.

Figure 2

BOLD responses in cortical regions along the parahippocampal gyrus. A) Brain regions of interest: top: perirhinal cortex; bottom: parahippocampal cortex. B) Comparisons of Scene + Object (S+O), Scene only (S) and Forgotten items (M). In perirhinal cortex, S+O differs from S (p = .05), no significant differences are seen in parahippocampal cortex. C) Comparisons in the same regions separating scene memory conditions into those subjectively reported as “Remember” (recollected) or ”Familiar”. In perirhinal cortex, Scene Remember + Object (SR+O) is significantly greater than Scene Remember only (SR), despite the fact that both scenes are judged remembered. This trend appears inverted in parahippocampal cortex with SR numerically greater than SR+O. (Abbreviations: S+O = Scene + Object; S = Scene Only; M = Forgotten items (Miss); SR+O = Scene Remember + Object; SR = Scene Remember Only; SF = Scene Familiar Only)

Figure 3

BOLD responses in Hippocampus. Plots show hemodynamic responses for four conditions (SR+O, SR, SF, and M). A) ROI in anterior hippocampus shows comparable activation for SR and SR+O suggesting content-general recollective effects. B) ROI in posterior hippocampus: SR shows significantly greater activation compared to all other conditions including SR+O. (Abbreviations: SR+O = Scene Remember + Object; SR = Scene Remember Only; SF = Scene Familiar Only; M = Forgotten items (Miss))

Figure 4

Region by condition interactions. Activation for SR+O and SR, remembered conditions that differ on subsequent object source recollection, were compared across different MTL regions. A) Comparison of perirhinal and parahippocampal cortices reveals a significant REGION by CONTENT interaction for SR+O and SR across the anterior perirhinal region and in the posterior parahippocampal region. B). Comparison of the same conditions in anterior hippocampus and posterior hippocampus reveals an interaction that trends towards significance (p = .06). (Abbreviations: SR+O = Scene Remember + Object; SR = Scene Remember Only; PR = perirhinal cortex; PH = parahippocampal cortex; HIP = hippocampus; Ant = anterior; Post = posterior)