High-resolution fMRI of Content-sensitive Subsequent Memory Responses in Human Medial Temporal Lobe

Abstract

The essential role of the medial temporal lobe (MTL) in long-term memory for individual events is well established, yet important questions remain regarding the mnemonic functions of the component structures that constitute the region. Within the hippocampus, recent functional neuroimaging findings suggest that formation of new memories depends on the den tate gyrus and the CA3 field, whereas the contribution of the subiculum may be limited to retrieval. During encoding, it has been further hypothesized that structures within MTL cortex contribute to encoding in a content-sensitive manner, whereas hippocampal structures may contribute to encoding in a more domain-general manner. In the current experiment, high-resolution fMRI techniques were utilized to assess novelty and subsequent memory effects in MTL subregions for two classes of stimuli—faces and scenes. During scanning, participants performed an incidental encoding (target detection) task with novel and repeated faces and scenes. Subsequent recognition memory was indexed for the novel stimuli encountered during scanning. Analyses revealed voxels sensitive to both novel faces and novel scenes in all MTL regions. However, similar percentages of voxels were sensitive to novel faces and scenes in perirhinal cortex, entorhinal cortex, and a combined region comprising the dentate gyrus, CA2, and CA3, whereas parahippocampal cortex, CA1, and subiculum demonstrated greater sensitivity to novel scene stimuli. Paralleling these findings, subsequent memory effects in perirhinal cortex were observed for both faces and scenes, with the magnitude of encoding activation being related to later memory strength, as indexed by a graded response tracking recognition confidence, whereas subsequent memory effects were scene-selective in parahippocampal cortex. Within the hippocampus, encoding activation in the subiculum correlated with subsequent memory for both stimulus classes, with the magnitude of encoding activation varying in a graded manner with later memory strength. Collectively, these findings suggest a gradient of content sensitivity from posterior (parahippocampal) to anterior (perirhinal) MTL cortex, with MTL cortical regions differentially contributing to successful encoding based on event content. In contrast to recent suggestions, the present data further indicate that the subiculum may contribute to successful encoding irrespective of event content.

Distinct Familiarity-Based Response Patterns for Faces and Buildings in Perirhinal and Parahippocampal Cortex

“…Images of chairs and buildings were obtained from the internet using Google Image Search. Images of faces were obtained from a database we acquired for another study (O'Neil et al, 2009). All visual background was removed from the target object depicted in each image and replaced by an artificial, homogenous background without any space-defining features (Fig.…”

“…Pertinent previous fMRI research suggests that participants can indeed control the extent to which they attempt to retrieve contextual details in recognition decisions strategically (Dobbins and Han, 2006;Quamme et al, 2010). The specific instructions were guided by those provided by Montaldi et al (2010; for additional rationale, see Migo et al, 2012). Participants were informed that, despite their efforts to focus on familiarity, spontaneous recollection could be ex- Figure 1.…”

“…Much pertinent research in human and nonhuman species has focused on recognition memory, i.e., the ability to discriminate between previously encountered and novel stimuli, and the question of whether different MTL structures make distinct functional contributions. An influential view is that the hippocampus (Hip) plays a unique role in the encoding and subsequent recovery of episodic contextual information about a specific previous stimulus encounter, whereas perirhinal cortex (PrC) supports recognition based on the familiarity of the item itself (Aggleton and Brown, 1999;Eichenbaum et al, 2007;Mayes et al, 2007). However, there are also findings that point to category-specific contributions of different MTL structures to recognition memory (Davachi, 2006;Murray et al, 2007;Graham et al, 2010).…”

“…An influential view is that the hippocampus (Hip) plays a unique role in the encoding and subsequent recovery of episodic contextual information about a specific previous stimulus encounter, whereas perirhinal cortex (PrC) supports recognition based on the familiarity of the item itself (Aggleton and Brown, 1999;Eichenbaum et al, 2007;Mayes et al, 2007). However, there are also findings that point to category-specific contributions of different MTL structures to recognition memory (Davachi, 2006;Murray et al, 2007;Graham et al, 2010). An important, currently unresolved question is how categoryspecific effects relate to the distinction between item-based and contextually based recognition processes.…”

“…Differential fMRI responses to faces are typically most pronounced in aspects of the lateral occipital and posterior fusiform gyrus (Kanwisher et al, 1997;for review, see Gobbini and Haxby, 2007) but have also been reported more rostrally in PrC (Tsao et al, 2008;Nasr and Tootell, 2012;O'Neil et al, 2013). In contrast, differential responses to scenes have been found predominantly in posterior aspects of PhC (Epstein and Kanwisher, 1998;Epstein, 2008).…”