As discussed in the Introductory chapter, there are competing accounts for how subregions in the MTL contribute to memory. According to a dual-process account (see Section 1.4), MTL subregions differentially contribute to recognition memory based upon recollection and familiarity (Aggleton & Brown, 1999; Brown & Aggleton, 2001), and there is now considerable evidence from the neuropsychological and neuroimaging literatures that links the perirhinal cortex and hippocampus to familiarity and recollection, respectively (Aggleton & Brown, 2005; Bowles et al., 2007; Cansino et al., 2002; Cohn et al., 2009; Daselaar et al., 2006; Davachi et al., 2003; Henson et al., 1999; Montaldi et al., 2006; Ranganath et al., 2004; Yonelinas et al., 1998; Yonelinas et al., 2002; Yonelinas et al., 2005). The vast majority of experiments have, however, used verbal stimuli (although see Montaldi et al., 2006) it is unclear, therefore, whether this division of applies to complex visual stimuli such as faces and scenes.
There are also recent representational accounts (see Section 1.6 and 1.7) which suggest that the kinds of stimuli employed in mnemonic and perceptual tasks separate the roles played by MTL subregions (Graham et al., 2010; see also Bussey & Saksida, 2005; Cowell et al., 2010; Saksida & Bussey, 2010). For example, according to the emergent memory account (EMA: Graham et al., 2010; see Section 1.7), subregions of the MTL differentially process representations of complex visual information, such as objects and scenes. Recent empirical findings have indicated that the perirhinal cortex is consistently associated with processing objects and faces, while the hippocampus processes scenes and is engaged by spatially demanding tasks (Awipi & Davachi, 2008; Barense et al., 2005; Barense et al., 2007; Barense, Henson et al., 2010; Kohler et al., 2005; Lee, Bandelow et al., 2006; Lee, Buckley et al., 2005; Lee, Bussey et al., 2005; Lee et al., 2008; Litman et al., 2009; Pihlajamaki et al., 2004;
E n c o d in g ( s c a n n e d ) Repeat Targe*
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Target Repeal Repeat
R e c o g n itio n ( n o t s c a n n e d ) ■ f T Participant’s Response 3 Hit
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CR FA Miss CR
High Conl. Low Conf. Low Conf. Low Conf.
Figure 2.1: Example o f the materials an d task design fro m Preston et al. (2010). (A) In the scanned encoding ph ase participants perform ed a target detection task on novel and repeated fa c e and scene stimuli. (B) During the unscanned test p h ase participants were p resen ted with novel stimuli fro m the encoding ph ase along with unstudied fa c e s and scenes. They responded to items using a 5 point confidence scale (1 = sure new; 2 = som ewhat sure new; 3 = unsure new; 4 = somewhat sure old; 5 = sure old).
Taylor et al., 2007; Rudebeck & Lee, 2010). It is currently unclear, however, whether a given MTL region will be recruited solely based upon the requirements posed by different stimulus types, or according to the processes that support memory judgements. It is also possible that recruitment of MTL subregions will be based
upon some interaction between stimulus and process (Graham et al., 2010).
How consistent are the predictions of EMA with the findings from previous fMRI studies that have directly contrasted long-term memory for different types of complex visual stimuli within the same experiment? In a comparison of recognition memory for faces and scenes, Preston at al. (2010) identified subsequent memory effects in the posterior parahippocampal cortex that were scene selective, but within the hippocampus and perirhinal cortex memory-related activity was domain-general (for similar domain-general effects at encoding and retrieval within the hippocampus see Prince et al., 2009). These data were interpreted as evidence against a strict stimulus- specific division of labour between MTL subregions. Importantly, however, while EMA claims that the perirhinal cortex is associated with processing object features and the hippocampus spatial features, these functional differences are not absolute.
For example, it is possible that the perirhinal cortex will be recruited to process individual objects within a scene (Graham et al., 2010). The scenes used by Preston et al. (2010) comprised indoor and outdoor scenes, most of which contained multiple distinctive objects (such as a dining room full o f tables and chairs, table settings and
floral centre pieces). Furthermore, during the scanned encoding phase, participants were required to detect a target scene and face, both of which were repeated 50 times across the run (Fig. 2.1). One effective target detection strategy could be to identify unique and salient objects within the scenes. Hence, the target detection task employed by Preston et al. (2010) could have encouraged participants to process object information in scenes.
Awipi and Davachi (2008) identified stimulus-specific brain activity at encoding that predicted recollection for objects in the perirhinal cortex and item memory for scenes in the posterior hippocampus and parahippocampal gyrus. Participants were presented with scenes that were paired with 1 of 6 repeating objects at encoding, their memory for which was assessed in a subsequent test phase (see Section 1.6.3). To identify content sensitive ‘recollection’ of the objects the authors compared encoding trials for which the scene was later remembered with and without the paired object. Importantly, the encoding task required participants to imagine using the object within the presented scene, which may have encouraged them to process the scene/object pair as a single unit. If they encoded a scene and object pair as a single unit (Diana et al., 2008; Haskins et al., 2008; Quamme et al., 2007; Yonelinas et al., 1999), old/new judgements, as well as accurate source judgments for these unitised pairings might be
made using familiarity (see also Mayes et al., 2007).
This object source memory effect was identified by making comparisons across conditions in which there was subsequent memory for different stimulus types (e.g. remembered object + scene > remembered scene). As a result, the activity for object/scene pairs in perirhinal cortex could merely reflect visual processing of the object or object viewing (Awipi & Davachi, 2008), which may relate indirectly to subsequent memory. As such, these effects could reflect stimulus-specific perceptual processing within the MTL (such as that seen in Barense, Henson et al., 2010; Devlin & Price, 2007; Lee, Bandelow et al., 2006), as opposed to subsequent recollection of the object (Awipi & Davachi, 2008). Stronger evidence of content sensitive recollection, therefore, could be derived by making comparisons between memory conditions for the same stimulus type (e.g. recollection of objects > familiarity for objects). These caveats, when coupled with the fact that these data also diverge from
those reported by Preston et al. (2010), emphasise the need for further investigation into the roles played by MTL subregions in memory for different stimulus types.
The current study was designed to re-examine long-term memory processing for faces and scenes within the MTL at encoding and also at retrieval, using a different encoding task and stimulus materials to those utilised by Preston et al. (2010). During a scanned encoding phase, participants were presented with novel faces and scenes and completed a pleasant/unpleasant task. The majority of the study materials comprised the face and scene stimuli from Taylor et al. (2007), who successfully demonstrated stimulus-specific memory deficits in MTL amnesia. Scenes that contained distinctive and/or numerous objects were not used, and the additional real- world scenes photographed for this experiment also contained few objects.
To identify stimulus-specific memory effects during retrieval, participants were also scanned during the test phase. At test, participants made memory judgments about the previously studied, and novel, faces and scenes. As confidence data have been used extensively to plot ROCs and compute behavioural estimates of recollection and familiarity (see Section 1.4.1.3; Yonelinas, 1994; Yonelinas, 2002), participants made memory judgements to test items on a 6-point scale that ranged from sure new through to sure old. If memory accuracy is greater for faces or scenes, or there are differences between recollection and/or familiarity estimates, stimulus-specific memory effects could reflect differences in how memorable one stimulus is over the other, and/or disproportionate dependence on the type of mnemonic processing supported by respective regions. This would, therefore, undermine the conclusion that any stimulus-specific activity reflects differences in processing and storing complex visual information used during memory encoding and retrieval. Likewise, if recollection and familiarity estimates for faces and scenes are equivalent, patterns of stimulus-specific memory activity within subregions of the MTL have important implications for dual-process accounts. Using the confidence data, it was also possible to observe'how patterns of memory-related activity within the MTL were modulated by increases in memory strength, and to infer how these patterns may map onto recollection and/or familiarity (Cohn et al., 2009; Daselaar et al., 2006; Ranganath et al., 2004; Yonelinas et al., 2005; also see Section 1.4.4).
Memory encoding and retrieval of faces and scenes were investigated within face and scene-sensitive functionally defined areas of the hippocampus, parahippocampal gyrus and perirhinal cortex. In keeping with the findings from the neuropsychological studies described previously (Lee, Buckley et al., 2005; Lee, Bussey et al., 2005; Taylor et al., 2007), and in keeping with a representational account, it is predicted that areas of the MTL that are more active when processing faces rather than scenes (e.g. perirhinal cortex) will also show a pattern of activity that relates to memory accuracy for faces, but not for scenes. The corresponding prediction for scenes, patterns of activity that track memory for scenes, applies to regions (e.g. posterior hippocampus) that are more active during the processing of scenes than faces. According to a dual process account (Aggleton & Brown, 1999; Brown & Aggleton, 2001), however, significant effects should be domain-general and patterns of memory-related activity in the hippocampus (as well as the posterior parahippocampal gyrus; Diana et al., 2007) and perirhinal cortex should differentially reflect recollection and familiarity, respectively. It is possible, however, that domain-general effects could appear stimulus-specific if memory for faces or scenes disproportionately relies on recollection or familiarity (e.g. a higher familiarity estimate for faces coupled with a face-specific memory effect in perirhinal cortex). As such, interpretations of stimulus-specific memory effects are contingent upon important aspects of the behavioural data (e.g. overall memory accuracy and ROC estimates for faces and scenes).