Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies
Research Highlights
► SM effects associated mostly with content processing, storage, and attention regions. ► SF effects associated mostly with default-mode network regions. ► The left IFC and fusiform cortex support content processing. ► The MTL supports storage operations ► The PMC and PPC support attention during encoding.
Introduction
On any given day, we encounter and experience many events. Only some of these experiences are transformed into memories and can be subsequently remembered. A key line of inquiry for students of memory concerns the neural activity predicting events that will be remembered, as opposed to those that will be forgotten. The advent of event-related functional magnetic resonance imaging (fMRI) made an extremely powerful paradigm for addressing this question possible (Brewer et al., 1998, Wagner et al., 1998, Wagner et al., 1998). In this paradigm, participants are presented with a series of encoding stimuli (trials), and encoding stimuli are sorted into those that would be remembered versus those that would be forgotten, based on participants' performances on a subsequent memory test. The fMRI signal that is greater for the stimuli later remembered than for those later forgotten (called a subsequent memory [SM] effect) indicates the presence of neural activity that supports successful encoding. The reverse situation, i.e., greater fMRI signal for the stimuli later forgotten than for those later remembered (called a subsequent forgetting (SF) effect), indicates neural activity that interferes with successful encoding. The SM paradigm, with its “compelling” operational definition of successful encoding activity, was very popular throughout the past decade. To date, over 100 fMRI studies have used the SM approach (Uncapher and Wagner, 2009). The present study aimed to provide the first comprehensive meta-analysis of such literature. This meta-analysis, though restricted to the literature examining visual information encoding in healthy young adults, considered both SM and SF effects.
In addition to the generic purpose of integrating results across studies, the present meta-analysis investigated several specific hypotheses regarding SM effects. After reviewing the relevant literature, comprising all published fMRI studies using an SM approach, we observed the emergence of two major study divisions. In one group of studies, the to-be-remembered material was verbal (e.g., words), while in the other group, it was pictorial (e.g., pictures, scenes, or faces). Further, one group of studies used item-memory tasks, while the other group used associative-memory tasks. In an item-memory task, participants try to remember an item with no other associated information, whereas in an associative-memory task, they must remember both an item and some information associated with that item, e.g., the context in which the item was presented (item–context association) or the fact that two items were presented as a pair (item–item association). Based on the reviewed studies' two divisions, the present meta-analysis compared (i) the SM effects of those studies using verbal versus pictorial material and (ii) the SM effects of those studies using item-memory versus associative-memory tasks. These comparisons cut across several critical issues relating to episodic encoding activity (see below).
Neuroimaging studies examining SM effects have traditionally focused on the prefrontal cortex (PFC) and the medial temporal lobe (MTL; Buckner et al., 2001, Fernandez and Tendolkar, 2001, Simons and Spiers, 2003). However, other brain regions, such as the fusiform cortex (Dickerson et al., 2007, Garoff et al., 2005, Kim and Cabeza, 2007), posterior parietal cortex (PPC; Sommer et al., 2005a, Sommer et al., 2005b, Uncapher and Rugg, 2009), and premotor cortex (PMC; Kao et al., 2005, Morcom et al., 2003) have been associated with SM effects. The multiple brain regions associated with SM effects may be broadly divided into three types, (i) content processing, (ii) storage, and (iii) attention. First, content processing regions mediate “the transformation of sensory input into internal representations that are interpreted or comprehended” (Paller and Wagner, 2002). The PFC, particularly the left inferior frontal cortex (IFC) and fusiform cortex are canonical examples of such regions (Kirchhoff et al., 2000). Second, storage regions bind the content representations into a durable memory representation, which the individual can access and retrieve into consciousness later. The MTL, and, in particular, the hippocampal formation, is widely recognized as the key structure in this function (Diana et al., 2007, Squire et al., 2004). Finally, attention during encoding selects an event among competing inputs and biases its “online” processing. A leading model of visual attention (Corbetta et al., 2002, Corbetta et al., 2008) has implicated a frontoparietal network, which includes the PMC and PPC, as a critical attention-coding structure. This three-component model does not represent a strict categorization of encoding-related activity, but rather some useful heuristics that can guide further research. For example, all regions displaying SM effects may have at least some relevance to storage.
As stated above, the present meta-analysis also compared SM effects between studies using verbal versus pictorial material. Historically, researchers have framed such comparisons and associated results in terms of hemispheric specialization or laterality effects (Golby et al., 2001, Kelley et al., 1998). This presupposes that verbal material encoding depends more on left- than right-hemispheric processing, whereas pictorial material encoding involves more right- than left-hemispheric processing. However, in the present meta-analysis, the primary purposes for this comparison were to address the following two hypotheses.
The first hypothesis states processing and successfully encoding either verbal or pictorial materials, which are canonically different in content, will emphasize different content-processing regions. Specifically, the left IFC, known to support controlled semantic/phonological retrieval and analysis (Badre and Wagner, 2007, Buckner et al., 1999), may be critical for successfully encoding verbal material, whereas the fusiform cortex, known to mediate visuoperceptual analysis and differentiation (Garoff et al., 2005, Kanwisher et al., 2001), may be critical for successfully encoding pictorial material.
Second, many SM studies have failed to find significant effects in the MTL (for a review, see Henson, 2005), despite the MTL's widely accepted critical role in storage operations. This failure remains largely unexplained, though researchers have attributed it to a low signal-to-noise ratio, susceptibility to MRI artifacts, or other nuisance factors. One relevant factor may be the widespread use of high frequency words, which participants had encountered numerous times prior to the studies, as encoding stimuli. Thus, participants had high pre-experimental familiarity with the verbal material, but not the pictorial material, used in SM studies. One influential view of the encoding process, known as the novelty-encoding hypothesis (Tulving et al., 1996), suggested the encoding system is biased toward processing novel, as opposed to familiar, information, because the system evolved to register information having high survival value. Thus, the second hypothesis addressed in this comparison is a novelty-encoding hypothesis predicting greater SM effects in the MTL during the encoding of pictorial material as compared to verbal material.
The present meta-analysis also compared SM effects between those studies using an item-memory task versus those with an associative-memory task. Historically, the distinction between item- versus associative-memory related to the distinction between familiarity (i.e., a feeling of “oldness” in the absence of contextual details) and recollection (i.e., vividly remembering specific contextual details). For example, a dual-process model of recognition memory suggested that associative recognition reflects recollection-based responses, whereas item recognition reflects both recollection- and familiarity-based responses (Yonelinas, 1997). The primary purposes for the present comparison of item- versus recognition-memory were to test the following two hypotheses.
First, prior discussions of the neural substrates for item- versus associative-memory predominantly focused on the MTL (Brown and Aggleton, 2001, Eichenbaum et al., 2007). A critical MTL function in episodic encoding is binding or associating multiple internal representations linked to an event, so the individual can retrieve the resultant representation as a whole (Davachi, 2006, Diana et al., 2007, Squire et al., 2004). Even though an item-memory task implicitly involves associating an item with spatiotemporal characteristics of the study episode, an associative-memory task makes stronger demands on associations, by requiring explicit item-context or item-item associations. Thus, the first hypothesis states MTL regions will show more robust SM effects during an associative-encoding task than during an item-encoding task.
Second, the distinction between item- and associative-memory, though traditionally focused on the MTL, may also involve differential SM effects in other brain regions (Kirwan et al., 2008). An associative-encoding task, as compared to an item-encoding task, typically makes greater content-processing demands, presenting multiple pieces of information and requiring relational processing among them. For example, an item–item association task may ask participants to rate how well two members of a pair (e.g., word–word) fit together (e.g., Qin et al., 2007) or to form a mental image incorporating both members of a pair and rate the quality of the image (e.g., Jackson and Schacter, 2004). By contrast, an item encoding task typically involves a relatively simple semantic (e.g., Is the word concrete or abstract?) or visual judgment (e.g., Is the face male or female?). Thus, the second hypothesis states content processing regions, such as left IFC and fusiform cortex, will exhibit stronger SM effects during associative versus item encoding.
Finally, encoding makes demands on attention, as shown by extensive behavioral evidence demonstrating that divided attention had negative effects on encoding (e.g., Craik et al., 1996). However, SM studies' explicit documentation of attention-related effects are relatively recent (Kensinger et al., 2003, Uncapher and Rugg, 2009, Uncapher and Rugg, 2008). A recent meta-analysis (Uncapher and Wagner, 2009) of relevant literature focused on the PPC as mediating attention during encoding. However, mounting evidence suggests attention does not depend on a single region but rather on a network of regions that interact with each other (for a review, see Raz and Buhle, 2006). Thus, attention during encoding is unlikely to involve a single region, but rather multiple regions, which include the frontal as well as the parietal cortex. Both a leading visual attention model (Corbetta et al., 2002, Corbetta et al., 2008) and meta-analyses of attention and working memory studies (Owen et al., 2005, Wager et al., 2004) suggest perhaps a frontoparietal network, including both the PMC and PPC, supports attention during encoding. Thus, the present meta-analysis investigated whether the PMC and PPC regions showed significant SM effects, and, if so, whether the nature of the material (verbal versus pictorial) and/or the type of encoding (item versus associative) modulated these SM effects.
Otten and Rugg (2001b) were the first to describe regions that showed SF effects, also called “reversed” or “negative” SM effects (Duverne et al., 2009, Weis et al., 2004). Their findings indicated SF effects were associated with widespread cortical regions, including the inferior parietal, medial parietal, posterior cingulate, and superior frontal cortices. At a minimum, these findings indicated that, to understand encoding, researchers must pay attention, not only to the positive correlates of remembering (SM effects), but also to the negative correlates of remembering (SF effects). Though relatively few fMRI studies have focused on SF effects, researchers generally accept the existence of cortical regions associated with SF effects (Park and Rugg, 2008, Shrager et al., 2008). Given the relatively limited number of available studies, the present meta-analysis focused mainly on general SF effects, involving the whole group, rather than specific SF effects restricted to a subgroup.
Multiple prior studies (Daselaar et al., 2004, Kim et al., 2010, Park and Rugg, 2008, Shrager et al., 2008, Turk-Browne et al., 2006) noted that the regions associated with SF effects tended to be components of what has been termed the default-mode network, which consists of the anterior and posterior midline cortex, the temporoparietal junction (TPJ), and the superior frontal cortex (Raichle et al., 2001). Based on this evidence, the present study examined whether, and to what extent, SF effects associate with default-mode network regions. The default-mode network was originally defined as the set of regions that are more active during the passive resting state than during attention-demanding cognitive tasks (Raichle et al., 2001, Shulman et al., 1997, Laird et al., 2009a). Researchers are currently debating these regions' functions, but increasing evidence suggests they mediate self-referential processing, or, more generally, internally oriented processing, as indicated by higher activations (or less deactivations) of these regions during imagining the future, conceiving the viewpoint of others (theory of mind), and autobiographical memory (for reviews, see Buckner and Carroll, 2007, Gusnard and Raichle, 2001, Spreng et al., 2009). Of greater direct relevance to SF effects, activation of these regions during an exogenous task may signal a wandering mind or momentary lapse of attention (Christoff et al., 2009, Mason et al., 2007, McKiernan et al., 2006, Weissman et al., 2006). For example, Christoff et al. (2009), using experience sampling during an fMRI task, found direct evidence for an association between activation of default-mode network regions and mind-wandering. Thus, activation of these regions during encoding may take neural resources away from the processes that lead to effective remembering.
The present study's principal methodology was a quantitative (i.e., statistical) meta-analysis of the relevant literature. A primary use for meta-analyses in neuroimaging is identifying significant concordances in brain activity patterns across a set of independent studies using a specific paradigm (Wager et al., 2007). The discernment of findings' convergences and divergences among studies is becoming increasingly important, albeit more difficult, as neuroimaging data continue to accumulate at a rapidly accelerating pace (Laird et al., 2009b). A quantitative meta-analysis provides an efficient and bias-free means of accomplishing this. The results of the present meta-analysis identify the brain regions most reliably associated with SM or SF effects and those most consistently exhibiting modulation of SM effects by the nature of the material and/or by the type of encoding. Of four recent meta-analyses of neuroimaging data that included SM studies, only one (Spaniol et al., 2009) used a quantitative approach; however, it employed a limited database (26 studies). The other three used a tabular method and focused exclusively on the MTL (Diana et al., 2007), PFC (Blumenfeld and Ranganath, 2007), or PPC (Uncapher and Wagner, 2009). Thus, the present study is the first quantitative meta-analysis of SM studies based on a comprehensive database and a whole-brain approach.
Section snippets
Study selection
Multiple literature searches via Pubmed were completed in order to isolate all fMRI studies reporting SM or SF effects. Additionally, a reference list check of recent neuroimaging memory study reviews (Diana et al., 2007, Spaniol et al., 2009, Uncapher and Wagner, 2009) was done to identify relevant studies not found by the online database search. These search results were filtered to include only studies that (i) included healthy, young participants, (ii) presented encoding material via visual
SM effects
Table 2 and Fig. 1 show the ALE meta-analysis results for all included studies (see supplementary material available online (Supplementary Fig. 1) for a series of coronal views). The results indicated SM effects were mainly associated with five regions: the left IFC, bilateral fusiform cortex, bilateral MTL, bilateral PMC, and bilateral PPC, in approximate order of decreasing spatial extent. The left IFC cluster (Brodmann area [BA] 44, 45, 46, 47) included both the anterior and posterior extent
SM effects
These results revealed that SM effects associated most consistently with five neural regions: left IFC, bilateral fusiform cortex, bilateral hippocampal formation, bilateral PMC, and bilateral PPC. Moreover, the SM effects' magnitude in these regions showed reliable modulation by the nature of the material (verbal or pictorial) and/or by encoding type (item or associative). As per the three-component model outlined in Introduction section, activation of the left IFC and fusiform cortex regions
Conclusions
The present study performed a meta-analysis of functional MRI studies using an SM approach. The meta-analysis of SM effects indicated they most consistently associated with five neural regions: the left IFC, bilateral fusiform cortex, bilateral hippocampal formation, bilateral PMC, and bilateral PPC. Comparisons of SM effects among the four subgroups of studies, formed by crossing two major study divisions (verbal versus pictorial material and item versus associative encoding), yielded three
Acknowledgments
This work was supported by a Daegu University research grant in 2010.
References (144)
- et al.
Left ventrolateral prefrontal cortex and the cognitive control of memory
Neuropsychologia
(2007) - et al.
Hippocampal-prefrontal encoding activation predicts whether words can be successfully recalled or only recognized
Behav. Brain Res.
(2006) - et al.
Self-projection and the brain
Trends Cogn. Sci.
(2007) - et al.
Recognition memory for studied words is determined by cortical activation differences at encoding but not during retrieval
NeuroImage
(2004) - et al.
Word frequency and subsequent memory effects studied using event-related fMRI
NeuroImage
(2003) - et al.
Assembling and encoding word representations: fMRI subsequent memory effects implicate a role for phonological control
Neuropsychologia
(2003) - et al.
The reorienting system of the human brain: from environment to theory of mind
Neuron
(2008) - et al.
When less means more: deactivations during encoding that predict subsequent memory
NeuroImage
(2004) Item, context and relational episodic encoding in humans
Curr. Opin. Neurobiol.
(2006)- et al.
fMRI evidence of word frequency and strength effects during episodic memory encoding
Cogn. Brain Res.
(2005)
Effects of aging on transient and sustained successful memory encoding activity
Neurobiol. Aging
Imaging recollection and familiarity in the medial temporal lobe: a three-component model
Trends Cogn. Sci.
Emotional context modulates subsequent memory effect
NeuroImage
Emotional context during encoding of neutral items modulates brain activation not only during encoding but also during recognition
NeuroImage
Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level
Brain Res. Bull.
Regional brain activations predicting subsequent memory success: an event-related fMRI study of the influence of encoding tasks
Cortex
The effect of word concreteness on recognition memory
NeuroImage
Cerebellar contributions to episodic memory encoding as revealed by fMRI
NeuroImage
Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior
Neuron
How default is the default mode of brain function?: further evidence from intrinsic BOLD signal fluctuations
Neuropsychologia
The neural origins of specific and general memory: the role of the fusiform cortex
Neuropsychologia
Thresholding of statistical maps in functional neuroimaging using the false discovery rate
NeuroImage
Data-driven clustering reveals a fundamental subdivision of the human cortex into two global systems
Neuropsychologia
Memory strength and repetition suppression: multimodal imaging of medial temporal cortical contributions to recognition
Neuron
Dissociation of the neural correlates of visual and auditory contextual encoding
Neuropsychologia
Perirhinal cortex supports encoding and familiarity-based recognition of novel associations
Neuron
Encoding activity in anterior medial temporal lobe supports subsequent associative recognition
NeuroImage
Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding
Neuron
Overlapping brain activity between episodic memory encoding and retrieval: roles of the task-positive and task-negative networks
NeuroImage
Lost in localization? The focus is meta-analysis
NeuroImage
Greater activation of the “default” brain regions predicts stop signal errors
NeuroImage
Feeling-of-knowing in episodic memory: an event-related fMRI study
NeuroImage
The visual word form area: expertise for reading in the fusiform gyrus
Trends Cogn. Sci.
Interrupting the “stream of consciousness”: an fMRI investigation
NeuroImage
Rest–stimulus interaction in the brain: a review
Trends Neurosci.
When more means less: neural activity related to unsuccessful memory encoding
Curr. Biol.
Observing the transformation of experience into memory
Trends Cogn. Sci.
Neural correlates of successful encoding of semantically and phonologically mediated inter-item associations
NeuroImage
Interaction of working memory and long-term memory in the medial temporal lobe
Cereb. Cortex
Neural correlates of verbal memory encoding during semantic and structural processing tasks
NeuroReport
Prefrontal cortex and long-term memory encoding: an integrative review of findings from neuropsychology and neuroimaging
Neuroscientist
Baseline brain activity fluctuations predict somatosensory perception in humans
Proc. Natl. Acad. Sci. U. S. A.
Making memories: brain activity that predicts how well visual experience will be remembered
Science
Recognition memory: what are the roles of the perirhinal cortex and hippocampus?
Nat. Rev. Neurosci.
Frontal cortex contributes to human memory formation
Nat. Neurosci.
Encoding processes during retrieval tasks
J. Cogn. Neurosci.
Sex differences in the neural basis of emotional memories
Proc. Natl. Acad. Sci. U. S. A.
Brain activity underlying encoding and retrieval of source memory
Cereb. Cortex
Experience sampling during fMRI reveals default network and executive system contributions to mind wandering
Proc. Natl. Acad. Sci. U. S. A.
Neural systems for visual orienting and their relationships to spatial working memory
J. Cogn. Neurosci.
Cited by (446)
Neurophysiological mechanisms of cognition in the developing brain: Insights from intracranial EEG studies
2023, Developmental Cognitive NeuroscienceObserving memory encoding while it unfolds: Functional interpretation and current debates regarding ERP subsequent memory effects
2023, Neuroscience and Biobehavioral Reviews