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

Abstract

An unresolved question in our understanding of the medial temporal lobes is how functional differences between structures pertaining to stimulus category relate to the distinction between item-based and contextually based recognition-memory processes. Specifically, it remains unclear whether perirhinal cortex (PrC) supports item-based familiarity signals for all stimulus categories or whether parahippocampal cortex (PhC) may also play a role for stimulus categories that are known to engage this structure in other task contexts. Here, we used multivoxel pattern analyses of fMRI data to compare patterns of activity in humans that are associated with the perceived familiarity of faces, buildings, and chairs. During scanning, participants judged the familiarity of previously studied and novel items from all three categories. Instances in which recognition was based on recollection were removed from all analyses. In right PrC, we found patterns of activity that distinguished familiar from novel faces. By contrast, in right PhC, we observed such patterns for buildings. Familiarity signals for chairs were present in both structures but shared little overlap with the patterns observed for faces and buildings on a more fine-grained scale. In the hippocampus, we found no evidence for familiarity signals for any object category. Our findings show that both PrC and PhC contribute to the assessment of item familiarity. They suggest that PhC does not only represent episodic context but can also represent item information for some object categories in recognition-memory decisions. In turn, our findings also indicate that the involvement of PrC in representing item familiarity is not ubiquitous.

Multivariate fMRI and Eye Tracking Reveal Differential Effects of Visual Interference on Recognition Memory Judgments for Objects and Scenes

“…This pattern of findings was not revealed in previous univariate analyses of the data, perhaps because of the reduced sensitivity of the univariate analysis approach with respect to small but reliable changes in activity (McIntosh & Lobaugh, 2004). Scene recognition, on the other hand, was associated with greater involvement of the parahippocampal gyrus around the third lag, with little reliable coactivity with prefrontal regions, consistent with the notion that scene familiarity may rely upon a different neural substrate than object familiarity (Martin, McLean, O'Neil, & Köhler, 2013). Importantly, the pattern displayed in the second LV does not indicate that there is an absence of prefrontal contributions during scene recognition, rather that coactivation of PRC with prefrontal regions during object recognition is more reliable.…”

“…PRC is often implicated to a greater extent in object recognition as compared to scene recognition (as reviewed in Ranganath & Ritchey, 2012;Diana, Yonelinas, & Ranganath, 2007;Eichenbaum, Yonelinas, & Ranganath, 2007;Davachi, 2006). For instance, a recent multivariate pattern analysis study has suggested that familiarity for objects may be supported by PRC-based representations, with scene recognition supported by the parahippocampal cortex (Martin et al, 2013), in line with the univariate findings reported by Watson and Lee (2013). Thus, differential recruitment of the network reported in this study following congruent and incongruent interference conditions for object, but not scene, recognition is in agreement with the view that the former is supported to a greater extent by PRC, whereas the latter is supported to a greater extent by parahippocampal cortex.…”

The Necessity of the Medial Temporal Lobe for Statistical Learning

“…Additionally, patients with selective hippocampal damage can have relatively intact item familiarity (Mayes, Holdstock, Isaac, Hunkin, & Roberts, 2002). Such familiarity may be supported by perirhinal cortex (Bowles et al, 2007; Eichenbaum, Yonelinas, & Ranganath, 2007; Brown & Aggleton, 2001) and parahippocampal cortex (Martin, McLean, O’Neil, & Kohler, 2013)—both of which are partially preserved in LSJ’s right hemisphere. Moreover, visual cortex exhibits attenuated responses to repeated versus novel stimuli, which may also support item familiarity (Turk-Browne, Yi, & Chun, 2006; Henson, Shallice, Gorno-Tempini, & Dolan, 2002).…”

Beyond the FFA: The role of the ventral anterior temporal lobes in face processing

“…Thus, it is not surprising that damage to the PrC in humans impairs face recognition (Lee, Bussey, et al, 2005; Martin, McLean, O'Neil, & Kohler, 2013). Notably, the PrC is preferentially activated when face discrimination places a higher demand on feature integration (O'neil et al, 2013) due to changes in the viewpoint from which faces are presented (Barense et al, 2010), or the presentation of faces with many, as opposed to few, overlapping features (Mundy, Downing, & Graham, 2012).…”

“…The PrC is preferentially sensitive to famous, as compared to unfamiliar faces (Barbeau et al, 2008; Barense et al, 2011; Martin et al, 2013) and damage to this region impairs one's ability to learn perceptual discriminations between highly similar faces (Mundy et al, 2013). Last, it has been reported that semantic memory deficits for concrete objects, most of which are defined by visual features, are associated with damage to the PrC and surrounding cortex (Mion et al, 2010).…”