Chapter 2
Functional Neuroimaging Approaches to Human Memory Junichi Chikazoe and Seiki Konishi
Abstract Historically, studies of brain-damaged humans and experimentally lesioned animals have provided abundant evidence regarding neural underpinning for episodic memory. These studies have revealed that the medial temporal lobe, including the hippocampus, plays a critical role in different memory stages including encoding, consolidation, and retrieval. Furthermore, these studies demonstrated differences in the level of impairment caused by a lesion across memory stages, suggesting that each stage might recruit different brain regions, although some of them might overlap. The advancement of neuroimaging methods such as functional magnetic resonance imaging (fMRI) enabled investigation of the thorough coverage of brain regions without invasion in healthy human subjects. In this chapter, we offer comprehensive and concise commentaries on functional neuroimaging approaches to reveal mechanisms underlying memory encoding, retrieval and consolidation. We further describe novel approaches such as multi-voxel pattern analysis used for decoding of memory representations and real-time fMRI that could show causality beyond correlation. Keywords Memory encoding • Memory retrieval • Memory consolidation • Multi- voxel pattern analysis • Real-time fMRI • Memory representation
2.1 Introduction In our daily life, we experience various events: seeing a cherry blossom, feeling a dull pain in a knee, listening to birdsong in the forest, etc. Even during the plainest day, some subtle signature of such events may be memorable. What determines whether an experience is later remembered or forgotten? Abundant evidence from behavioral neuropsychological studies has demonstrated that each stage of the J. Chikazoe (*) Section of Brain Function Information, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan e-mail:
[email protected] S. Konishi Department of Neurophysiology, Juntendo University School of Medicine, Tokyo, Japan © Springer Japan KK 2017 T. Tsukiura, S. Umeda (eds.), Memory in a Social Context, https://doi.org/10.1007/978-4-431-56591-8_2
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memory process is supported by partially overlapped but considerably distinct brain regions (Squire 1982). For example, neuropsychological studies revealed that patients with medial temporal lobe (MTL) damage had severe difficulty in encoding memory for novel events, whereas they could recall events that occurred before the traumatic event/surgery to some extent (Scoville and Milner 1957). Furthermore, memory loss caused by hippocampal damage showed a characteristic feature: the patients had difficulty in recalling events that had occurred recently, but they could recall older events (Scoville and Milner 1957). This feature, which is called “temporal gradient,” suggested that memories from the hippocampus might be moved to the neo-cortex in a more stabilized form of storage (memory consolidation) (Squire and Alvarez 1995). Although evidence from patients with brain damage is strong, they lack spatial resolution: in most cases, the damaged region is not localized, and it sometimes involves a broad range of brain areas that may have different functions. Moreover, the precise influence of a lesion on each memory stage (i.e., encoding, consolidation, and retrieval) is difficult to specify, which makes the role of a brain region for each memory stage ambiguous. In contrast, neuroimaging techniques such as functional magnetic resonance imaging (fMRI) has higher spatial resolution whereby functional organization on a subcentimeter scale can be detected (Hirose et al. 2009). Importantly, fMRI allows separation across memory stages. In this chapter, we describe a variety of task designs and analyses aimed at unveiling neural correlates of memory at each stage. We further refer to recent techniques such as controlling participants’ memory performance by modifying the timing of stimulus presentation based on online analysis of neuroimaging data, which is called “real- time fMRI.”
2.2 Encoding Neural correlates underlying memory encoding have been intensively investigated for decades. An experimental paradigm, the so-called subsequent memory paradigm, enabled comparing brain activity for items that are remembered or forgotten in a memory test, thus establishing a direct link between brain activity and successful memory formation (Dolcos et al. 2012; Wagner et al. 1998). In this paradigm, brain activity during the encoding phase is recorded and then trials were sorted, based on whether to be remembered or forgotten in the later memory test. By calculating the difference in brain activity associated with the later remembered and forgotten items, one can detect brain regions that mediate processes required for successful memory encoding (Paller et al. 1987). The fMRI signal that is greater for the items later remembered than for those later forgotten indicates the contribution of those regions to successful encoding (a subsequent memory [SM] effect). With this paradigm, neuroimaging studies revealed the SM effects in multiple brain regions, including the prefrontal cortex and medial temporal lobe (MTL) (Fernandez and Tendolkar 2001; Simons and Spiers 2003; Wagner et al. 1998) along with the fusiform cortex (Dickerson et al. 2007; Garoff et al. 2005; Kim and Cabeza 2007) and posterior parietal cortex (Sommer et al. 2005; Uncapher and Rugg 2009).
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Interestingly, several previous studies (Daselaar et al. 2004; Kim et al. 2010) reported that the subsequent memory performance was predicted by the deactivation of the default-mode network (a negative subsequent memory) (Duverne et al. 2009; Otten and Rugg 2001), which consists of the anterior and posterior midline cortex, the temporoparietal junction, and the superior frontal cortex (Raichle et al. 2001). A meta-analysis of 74 fMRI studies statistically confirmed those results and further revealed that the activation of the inferior frontal cortex was lateralized to the left hemisphere, whereas the other regions showed bilateral activation (Kim 2011). In this meta-analysis, the hemispheric laterality of the deactivation was found in the temporoparietal junction: temporoparietal deactivation was stronger in the right than in the left hemisphere. The meaning of the negative SM effects (i.e., forgotten > remembered) remains unclear. One possible explanation is that it may indicate greater activity interfering with successful encoding. Indeed, the default- mode network is known to be associated with mind-wandering during the task (Mason et al. 2007), which may interfere with the memory encoding of external events. Another possibility is that it may reflect a momentary lapse of attention. Previous attention studies demonstrated that less efficient stimulus processing during attentional lapses was characterized by less deactivation of the default-mode network (Weissman et al. 2006). From this perspective, greater deactivation predicting items remembered later may reflect the extent of attention allocated to the item.
2.3 Retrieval Neural correlates related to memory retrieval can be investigated using two standard approaches. It depends on the processes of interest which approach is preferable. The first approach is aimed at revealing “retrieval success,” which refers to processes that are selectively engaged when a retrieval attempt is successful (Rugg et al. 1996). The second approach is based on a “dual-process” model of memory (Yonelinas 2002). This model posits that a retrieval cue can elicit two qualitatively distinct kinds of mnemonic information, that is, recollection and familiarity (Rugg and Vilberg 2013). Recollection signal provides information about qualitative aspects of the past event, such as context or source of information whereas familiarity signal can support simple judgments of occurrence of the event. We demonstrate how to specify neural correlates of memory retrieval in addition to these two approaches.
2.3.1 Retrieval Success Neuroimaging studies can specify brain regions associated with a certain cognitive component by contrasting at least two conditions. For example, to retrieve memory from a visual word cue, visual and language systems should be recruited besides
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memory systems. If we assume that these systems would not interact with each other, we can hypothetically obtain a brain activation map of memory retrieval by subtracting the control condition (visual + language) from the target condition (visual + language + memory retrieval). In the case of the memory test, there are four conditions: hit (remembered old item), miss (forgotten old item), false alarm (new item incorrectly labeled as old), and correct rejection (new time correctly labeled as new). Apparently the “hit” condition is associated with successful retrieval; however, which condition to use for the control condition may depend on the research question. For example, to directly compare brain responses for the same stimuli between encoding and retrieval, some studies used the “miss” condition for the control (Huijbers et al. 2013). However, most studies used the “correct rejection” condition for the control, as this condition is thought to share similar cognitive components with “hit” except retrieval success (Tulving 1999). Interestingly, the contrast “hit versus correct rejection” has consistently revealed the involvement of the parietal lobe, including the lateral posterior parietal cortex, precuneus, and the mid-cingulate cortex (Kahn et al. 2004; Konishi et al. 2000; Wheeler and Buckner 2004). This result was surprising as the parietal lobe was not thought to support declarative memory previously (Wagner et al. 2005); however, it has been consistently reported by fMRI studies of memory retrieval from various laboratories (Konishi et al. 2000; McDermott et al. 2000; Spaniol et al. 2009; Wheeler and Buckner 2004). Resting state functional connectivity studies have consistently reported that these three regions form a functional network. In resting state functional connectivity analysis, low-frequency (
