Material Specificity Drives Medial Temporal Lobe Familiarity But Not Hippocampal Recollection

Abstract

The specific role of the perirhinal (PRC), entorhinal (ERC) and parahippocampal cortices (PHC) in supporting familiarity-based recognition remains unknown. An fMRI study explored whether these medial temporal lobe (MTL) structures responded in the same way or differentially to familiarity as a function of stimulus type at recognition. A secondary aim was to explore whether the hippocampus responds in the same way to equally strong familiarity and recollection and whether this is influenced by the kind of stimulus involved. Univariate and multivariate analyses revealed that familiarity responses in the PRC, ERC, PHC and the amygdala are material-specific. Specifically, the PRC and ERC selectively responded to object familiarity, while the PHC responded to both object and scene familiarity. The amygdala only responded to familiarity memory for faces. The hippocampus did not respond to stimulus familiarity for any of the three types of stimuli, but it did respond to recollection for all three types of stimuli. This was true even when recollection was contrasted to equally accurate familiarity. Overall, the findings suggest that the role of the MTL neocortices and the amygdala in familiarity-based recognition depends on the kind of stimulus in memory, whereas the role of the hippocampus in recollection is independent of the type of cuing stimulus. © 2016 The Authors Hippocampus Published by Wiley Periodicals, Inc.

Keywords: amygdala; entorhinal cortex; parahippocampal cortex; perirhinal cortex; recognition memory.

Figure 1

Experimental design and behavioral data. (A) Design of the fMRI experiment and sequence of trials at encoding and retrieval (scanned). Three types of stimuli (scenes, objects and faces) were studied at encoding and were later presented at retrieval (along with unstudied stimuli). Participants were asked to provide familiarity (F1, F2, F3), new (N) and recollection (R) responses for each stimulus. (B) Accuracy [Hits/(Hits + FAs)] collapsed across the three types of stimuli and separately for scenes, objects and faces. Recollection responses to faces were very rare and therefore are not reported separately. Error bars show the standard error of the mean. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 2

Material‐specific familiarity effects for (A) scenes, (B) faces and (C) objects in the MTL, the amygdala and the fusiform gyrus. Error bars show the standard error of the mean. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3

(A) Multivariate pattern recognition classification accuracy and (B) confusion matrices for the classification of strong familiarity (F3) responses within the perirhinal cortex (PRC), the entorhinal cortex (ERC), the parahippocampal cortex (PHC), the amygdala and the hippocampus for each stimulus type. Dashed lines in the graphs mark chance classification. Error bars indicate the standard error of the mean across participants. * P < 0.05; ** P < 0.01. P‐values were obtained through permutation testing with 1000 permutations.

Figure 4

Recollection selective response in the hippocampus for (A) scenes, (B) objects and (C) collapsed across scenes, objects and faces. (D) Selective parahippocampal cortex effect for R _scenes versus R _objects. Error bars show the standard error of the mean. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 5

Multivariate pattern recognition classification accuracy for R and F3 responses in the hippocampus, the perirhinal cortex (PRC), the entorhinal cortex, the parahippocampal cortex (PHC) and the amygdala. Error bars indicate the standard error of the mean across participants. * P < 0.05; ** P < 0.01; *** P < 0.001; † P = 0.08 (trend). P‐values were obtained through permutation testing with 1000 permutations.