A meta-analysis of event-related potential correlates of recognition memory.

A longstanding question in memory research is whether recognition is supported by more than one mnemonic process. Dual-process models distinguish recollection of episodic detail from familiarity, while single-process models explain recognition in terms of one process that varies in strength. Dual process models have drawn support from findings that recollection and familiarity elicit distinct electroencephalographic event-related potentials (ERPs): a mid-frontal ERP effect that occurs at around 300-500 ms post-stimulus onset and is often larger for familiarity than recollection contrasts, and a parietal ERP effect that occurs at around 500-800 ms and is larger for recollection than familiarity contrasts. We sought to adjudicate between dual- and single-process models by investigating whether the dissociation between these two ERP effects is reliable over studies. We extracted effect sizes from 41 experiments that had used Remember-Know, source memory, and associative memory paradigms (1,000 participants). Meta-analysis revealed a strong interaction between ERP effect and mnemonic process of the form predicted by dual-process models. Although neither ERP effect was significantly process-selective taken alone, a moderator analysis revealed a larger mid-frontal effect for familiarity than recollection contrasts in studies using the Remember-Know paradigm. Mega-analysis of raw data from six studies further showed significant process-selectivity for both mid-frontal and parietal ERPs in the predicted time windows. On balance, the findings favor dual- over single-process theories of recognition memory, but point to a need to promote sharing of raw data.

Cue overlap supports preretrieval selection in episodic memory: ERP evidence.

People often want to recall events of a particular kind, but this selective remembering is not always possible. We contrasted two candidate mechanisms: the overlap between retrieval cues and stored memory traces, and the ease of recollection. In two preregistered experiments (Ns = 28), we used event-related potentials (ERPs) to quantify selection occurring before retrieval and the goal states - retrieval orientations - thought to achieve this selection. Participants viewed object pictures or heard object names, and one of these sources was designated as targets in each memory test. We manipulated cue overlap by probing memory with visual names (Experiment 1) or line drawings (Experiment 2). Results revealed that regardless of which source was targeted, the left parietal ERP effect indexing recollection was selective when test cues overlapped more with the targeted than non-targeted information, despite consistently better memory for pictures. ERPs for unstudied items also were more positive-going when cue overlap was high, suggesting that engagement of retrieval orientations reflected availability of external cues matching the targeted source. The data support the view that selection can act before recollection if there is sufficient overlap between retrieval cues and targeted versus competing memory traces.

Does Hemispheric Asymmetry Reduction in Older Adults in Motor Cortex Reflect Compensation?

Older adults tend to display greater brain activation in the nondominant hemisphere during even basic sensorimotor responses. It is debated whether this hemispheric asymmetry reduction in older adults (HAROLD) reflects a compensatory mechanism. Across two independent fMRI experiments involving adult life span human samples (N = 586 and N = 81, approximately half female) who performed right-hand finger responses, we distinguished between these hypotheses using behavioral and multivariate Bayes (MVB) decoding approaches. Standard univariate analyses replicated a HAROLD pattern in motor cortex, but in and out of scanner behavioral results both demonstrated evidence against a compensatory relationship in that reaction time measures of task performance in older adults did not relate to ipsilateral motor activity. Likewise, MVB showed that this increased ipsilateral activity in older adults did not carry additional information, and if anything, combining ipsilateral with contralateral activity patterns reduced action decoding in older adults (at least in experiment 1). These results contradict the hypothesis that HAROLD is compensatory and instead suggest that the age-related ipsilateral hyperactivation is nonspecific, consistent with alternative hypotheses about age-related reductions in neural efficiency/differentiation or interhemispheric inhibition.SIGNIFICANCE STATEMENT A key goal in the cognitive neuroscience of aging is to provide a mechanistic explanation of how brain-behavior relationships change with age. One interpretation of the common finding that task-based hemispheric activity becomes more symmetrical in older adults is that this shift reflects a compensatory mechanism, with the nondominant hemisphere needing to help out with computations normally performed by the dominant hemisphere. Contrary to this view, our behavioral and brain data indicate that the additional activity in ipsilateral motor cortex in older adults is not reflective of better task performance nor better neural representations of finger actions.

Perceptual and Semantic Representations at Encoding Contribute to True and False Recognition of Objects.

When encoding new episodic memories, visual and semantic processing is proposed to make distinct contributions to accurate memory and memory distortions. Here, we used fMRI and preregistered representational similarity analysis to uncover the representations that predict true and false recognition of unfamiliar objects. Two semantic models captured coarse-grained taxonomic categories and specific object features, respectively, while two perceptual models embodied low-level visual properties. Twenty-eight female and male participants encoded images of objects during fMRI scanning, and later had to discriminate studied objects from similar lures and novel objects in a recognition memory test. Both perceptual and semantic models predicted true memory. When studied objects were later identified correctly, neural patterns corresponded to low-level visual representations of these object images in the early visual cortex, lingual, and fusiform gyri. In a similar fashion, alignment of neural patterns with fine-grained semantic feature representations in the fusiform gyrus also predicted true recognition. However, emphasis on coarser taxonomic representations predicted forgetting more anteriorly in the anterior ventral temporal cortex, left inferior frontal gyrus and, in an exploratory analysis, left perirhinal cortex. In contrast, false recognition of similar lure objects was associated with weaker visual analysis posteriorly in early visual and left occipitotemporal cortex. The results implicate multiple perceptual and semantic representations in successful memory encoding and suggest that fine-grained semantic as well as visual analysis contributes to accurate later recognition, while processing visual image detail is critical for avoiding false recognition errors.SIGNIFICANCE STATEMENT People are able to store detailed memories of many similar objects. We offer new insights into the encoding of these specific memories by combining fMRI with explicit models of how image properties and object knowledge are represented in the brain. When people processed fine-grained visual properties in occipital and posterior temporal cortex, they were more likely to recognize the objects later and less likely to falsely recognize similar objects. In contrast, while object-specific feature representations in fusiform gyrus predicted accurate memory, coarse-grained categorical representations in frontal and temporal regions predicted forgetting. The data provide the first direct tests of theoretical assumptions about encoding true and false memories, suggesting that semantic representations contribute to specific memories as well as errors.

Increased Prefrontal Activity with Aging Reflects Nonspecific Neural Responses Rather than Compensation.

Elevated prefrontal cortex activity is often observed in healthy older adults despite declines in their memory and other cognitive functions. According to one view, this activity reflects a compensatory functional posterior-to-anterior shift, which contributes to maintenance of cognitive performance when posterior cortical function is impaired. Alternatively, the increased prefrontal activity may be less efficient or less specific because of structural and neurochemical changes accompanying aging. These accounts are difficult to distinguish on the basis of average activity levels within brain regions. Instead, we used a novel, model-based multivariate analysis technique applied to two independent fMRI datasets from an adult-lifespan human sample (N = 123 and N = 115; approximately half female). Standard analysis replicated the age-related increase in average prefrontal activation, but multivariate tests revealed that this activity did not carry additional information. The results contradict the hypothesis of a compensatory posterior-to-anterior shift. Instead, they suggest that the increased prefrontal activation reflects reduced efficiency or specificity rather than compensation.SIGNIFICANCE STATEMENT Functional brain imaging studies have often shown increased activity in prefrontal brain regions in older adults. This has been proposed to reflect a compensatory shift to greater reliance on prefrontal cortex (PFC), helping to maintain cognitive function. Alternatively, activity may become less specific as people age. This is a key question in the neuroscience of aging. In this study, we used novel tests of how different brain regions contribute to long- and short-term memory. We found increased activity in PFC in older adults, but this activity carried less information about memory outcomes than activity in visual regions. These findings are relevant for understanding why cognitive abilities decline with age, suggesting that optimal function depends on successful brain maintenance rather than compensation.

Age-related changes in the neural networks supporting semantic cognition: A meta-analysis of 47 functional neuroimaging studies.

Semantic cognition is central to understanding of language and the world and, unlike many cognitive domains, is thought to show little age-related decline. We investigated age-related differences in the neural basis of this critical cognitive domain by performing an activation likelihood estimation (ALE) meta-analysis of functional neuroimaging studies comparing young and older people. On average, young people outperformed their older counterparts during semantic tasks. Overall, both age groups activated similar left-lateralised regions. However, older adults displayed less activation than young people in some elements of the typical left-hemisphere semantic network, including inferior prefrontal, posterior temporal and inferior parietal cortex. They also showed greater activation in right frontal and parietal regions, particularly those held to be involved in domain-general controlled processing, and principally when they performed more poorly than the young. Thus, semantic processing in later life is associated with a shift from semantic-specific to domain-general neural resources, consistent with the theory of neural dedifferentiation, and a performance-related reduction in prefrontal lateralisation, which may reflect a response to increased task demands.

Aging, working memory capacity and the proactive control of recollection: An event-related potential study.

The present study investigated the role of working memory capacity (WMC) in the control of recollection in young and older adults. We used electroencephalographic event-related potentials (ERPs) to examine the effects of age and of individual differences in WMC on the ability to prioritize recollection according to current goals. Targets in a recognition exclusion task were words encoded using two alternative decisions. The left parietal ERP old/new effect was used as an electrophysiological index of recollection, and the selectivity of recollection measured in terms of the difference in its magnitude according to whether recognized items were targets or non-targets. Young adults with higher WMC showed greater recollection selectivity than those with lower WMC, while older adults showed nonselective recollection which did not vary with WMC. The data suggest that aging impairs the ability to engage cognitive control effectively to prioritize what will be recollected.

Dopamine and memory dedifferentiation in aging.

The dedifferentiation theory of aging proposes that a reduction in the specificity of neural representations causes declines in complex cognition as people get older, and may reflect a reduction in dopaminergic signaling. The present pharmacological fMRI study investigated episodic memory-related dedifferentiation in young and older adults, and its relation to dopaminergic function, using a randomized placebo-controlled double-blind crossover design with the agonist Bromocriptine (1.25mg) and the antagonist Sulpiride (400mg). We used multi-voxel pattern analysis to measure memory specificity: the degree to which distributed patterns of activity distinguishing two different task contexts during an encoding phase are reinstated during memory retrieval. As predicted, memory specificity was reduced in older adults in prefrontal cortex and in hippocampus, consistent with an impact of neural dedifferentiation on episodic memory representations. There was also a linear age-dependent dopaminergic modulation of memory specificity in hippocampus reflecting a relative boost to memory specificity on Bromocriptine in older adults whose memory was poorer at baseline, and a relative boost on Sulpiride in older better performers, compared to the young. This differed from generalized effects of both agents on task specificity in the encoding phase. The results demonstrate a link between aging, dopaminergic function and dedifferentiation in the hippocampus.

Effects of perceptual similarity but not semantic association on false recognition in aging.

This study investigated semantic and perceptual influences on false recognition in older and young adults in a variant on the Deese-Roediger-McDermott paradigm. In two experiments, participants encoded intermixed sets of semantically associated words, and sets of unrelated words. Each set was presented in a shared distinctive font. Older adults were no more likely to falsely recognize semantically associated lure words compared to unrelated lures also presented in studied fonts. However, they showed an increase in false recognition of lures which were related to studied items only by a shared font. This increased false recognition was associated with recollective experience. The data show that older adults do not always rely more on prior knowledge in episodic memory tasks. They converge with other findings suggesting that older adults may also be more prone to perceptually-driven errors.

Cortical pattern separation and item-specific memory encoding.

Pattern separation and pattern completion are fundamental brain processes thought to be critical for episodic memory encoding and retrieval, and for discrimination between similar memories. These processes are best understood in the hippocampus, but are proposed to occur throughout the brain, in particular in sensory regions. Cortical, as well as hippocampal, pattern separation may therefore support formation of event-unique memory traces. Using fMRI, we investigated cortical pattern separation and pattern completion and their relationship to encoding activity predicting subsequent item-specific compared to gist memory. During scanning, participants viewed images of novel objects, repeated objects, and objects which were both perceptually and conceptually similar to previously presented images, while performing a size judgement task. In a later surprise recognition test, they judged whether test items were 'same' 'similar' or 'new' relative to studied items. Activity consistent with pattern separation - responses to similar items as if novel - was observed in bilateral occipito-temporal cortex. Activity consistent with pattern completion - responses to similar items as if repeated - was observed in left prefrontal cortex and hippocampus. Curve fitting analysis further revealed that graded responses to change in image conceptual and perceptual similarity in bilateral prefrontal and right parietal regions met specific computational predictions for pattern separation for one or both of these similarity dimensions. Functional overlap between encoding activity predicting subsequent item-specific recognition and pattern separation activity was also observed in left occipital cortex and bilateral inferior frontal cortex. The findings suggest that extrahippocampal regions including sensory and prefrontal cortex contribute to pattern separation and pattern completion of visual input, consistent with the proposal that cortical pattern separation contributes to formation of item-specific memory traces, facilitating accurate recognition memory.

Resisting false recognition: An ERP study of lure discrimination.

There is keen interest in what enables rememberers to differentiate true from false memories and which strategies are likely to be the most effective. This study measured electrical brain activity while healthy young adults performed a mnemonic discrimination task, deciding whether color pictures had been studied, were similar to studied pictures (lures), or were new. Between 500 and 800 ms post-stimulus, event-related potentials (ERPs) for correctly recognized studied pictures and falsely recognized lures compared to those for correctly rejected novel items had a left centroparietal scalp distribution. This was typical of the parietal old/new effect associated with recollection, and in line with previous evidence that similar lures may elicit false or phantom recollection as opposed to just familiarity. There was no evidence of a parietal effect for correctly rejected lures as would be expected if recall-to-reject was used. The ERP old/new effects for lures also varied with individual differences in performance. Parietal effects for falsely recognized lures were larger in better performers, who successfully rejected a greater number of lures as "similar". The better performers also showed more pronounced right frontocentral old/new effects between 800 and 1100 ms for correctly rejected and falsely recognized similar lures. The enhancement of false recollection in better performers implies false recognition of lures occurred only when more specific information was recovered about the study episodic. Together, the findings suggest reliance on recollection to decide that items were studied, supported by post-retrieval processing.

Neural reorganization and compensation in aging.

According to prominent theories of aging, the brain may reorganize to compensate for neural deterioration and prevent or offset cognitive decline. A frequent and striking finding in functional imaging studies is that older adults recruit additional regions relative to young adults performing the same task. This is often interpreted as evidence for functional reorganization, suggesting that, as people age, different regions or networks may support the same cognitive functions. Associations between additional recruitment and better performance in older adults have led to the suggestion that the additional recruitment may contribute to preserved cognitive function in old age and may explain some of the variation among individuals in preservation of function. However, many alternative explanations are possible, and recent findings and methodological developments have highlighted the need for more systematic approaches to determine whether reorganization occurs with age and whether it benefits performance. We reevaluate current evidence for compensatory functional reorganization in the light of recent moves to address these challenges.

Age-related increases in false recognition: the role of perceptual and conceptual similarity.

Older adults (OAs) are more likely to falsely recognize novel events than young adults, and recent behavioral and neuroimaging evidence points to a reduced ability to distinguish overlapping information due to decline in hippocampal pattern separation. However, other data suggest a critical role for semantic similarity. Koutstaal et al. [(2003) false recognition of abstract vs. common objects in older and younger adults: testing the semantic categorization account, J. Exp. Psychol. Learn. 29, 499-510] reported that OAs were only vulnerable to false recognition of items with pre-existing semantic representations. We replicated Koutstaal et al.'s (2003) second experiment and examined the influence of independently rated perceptual and conceptual similarity between stimuli and lures. At study, young and OAs judged the pleasantness of pictures of abstract (unfamiliar) and concrete (familiar) items, followed by a surprise recognition test including studied items, similar lures, and novel unrelated items. Experiment 1 used dichotomous "old/new" responses at test, while in Experiment 2 participants were also asked to judge lures as "similar," to increase explicit demands on pattern separation. In both experiments, OAs showed a greater increase in false recognition for concrete than abstract items relative to the young, replicating Koutstaal et al.'s (2003) findings. However, unlike in the earlier study, there was also an age-related increase in false recognition of abstract lures when multiple similar images had been studied. In line with pattern separation accounts of false recognition, OAs were more likely to misclassify concrete lures with high and moderate, but not low degrees of rated similarity to studied items. Results are consistent with the view that OAs are particularly susceptible to semantic interference in recognition memory, and with the possibility that this reflects age-related decline in pattern separation.

Moving to music: effects of heard and imagined musical cues on movement-related brain activity.

Music is commonly used to facilitate or support movement, and increasingly used in movement rehabilitation. Additionally, there is some evidence to suggest that music imagery, which is reported to lead to brain signatures similar to music perception, may also assist movement. However, it is not yet known whether either imagined or musical cueing changes the way in which the motor system of the human brain is activated during simple movements. Here, functional magnetic resonance imaging was used to compare neural activity during wrist flexions performed to either heard or imagined music with self-pacing of the same movement without any cueing. Focusing specifically on the motor network of the brain, analyses were performed within a mask of BA4, BA6, the basal ganglia (putamen, caudate, and pallidum), the motor nuclei of the thalamus, and the whole cerebellum. Results revealed that moving to music compared with self-paced movement resulted in significantly increased activation in left cerebellum VI. Moving to imagined music led to significantly more activation in pre-supplementary motor area (pre-SMA) and right globus pallidus, relative to self-paced movement. When the music and imagery cueing conditions were contrasted directly, movements in the music condition showed significantly more activity in left hemisphere cerebellum VII and right hemisphere and vermis of cerebellum IX, while the imagery condition revealed more significant activity in pre-SMA. These results suggest that cueing movement with actual or imagined music impacts upon engagement of motor network regions during the movement, and suggest that heard and imagined cues can modulate movement in subtly different ways. These results may have implications for the applicability of auditory cueing in movement rehabilitation for different patient populations.

Re-engaging with the past: recapitulation of encoding operations during episodic retrieval.

Recollection of events is accompanied by selective reactivation of cortical regions which responded to specific sensory and cognitive dimensions of the original events. This reactivation is thought to reflect the reinstatement of stored memory representations and therefore to reflect memory content, but it may also reveal processes which support both encoding and retrieval. The present study used event-related functional magnetic resonance imaging to investigate whether regions selectively engaged in encoding face and scene context with studied words are also re-engaged when the context is later retrieved. As predicted, encoding face and scene context with visually presented words elicited activity in distinct, context-selective regions. Retrieval of face and scene context also re-engaged some of the regions which had shown successful encoding effects. However, this recapitulation of encoding activity did not show the same context selectivity observed at encoding. Successful retrieval of both face and scene context re-engaged regions which had been associated with encoding of the other type of context, as well as those associated with encoding the same type of context. This recapitulation may reflect retrieval attempts which are not context-selective, but use shared retrieval cues to re-engage encoding operations in service of recollection.

Neural correlates of shape-color binding in visual working memory.

The present study addressed an outstanding issue regarding feature binding in working memory (WM): whether this function engages specific resources relative to those required to process individual features. We investigated the brain regions supporting the encoding and maintenance of features and bindings in a change detection task, in which 22 healthy young volunteers remembered visual arrays of abstract shapes, colors or shape-color bindings while undergoing fMRI. After an unfilled delay they saw a second array and judged whether the features or combination of features presented across the two arrays were the same or different. Temporary retention of feature bindings was found to involve additional cortical regions compared with retaining single features, regardless of whether the number of objects or the number of features differed between feature-only and binding conditions. This binding-specific activation is consistent with the involvement of different neural generators that collectively support visual temporary memory for features and for feature bindings. Regions within the parietal, temporal and occipital cortex, but not within the prefrontal cortex or the medial temporal lobe, appear to support the integrated object binding function investigated in this study. Our findings suggest that both individual features and their binding within integrated objects are used to represent complex objects in WM.

Retrieval orientation and the control of recollection: an fMRI study.

This study used event-related fMRI to examine the impact of the adoption of different retrieval orientations on the neural correlates of recollection. In each of two study-test blocks, participants encoded a mixed list of words and pictures and then performed a recognition memory task with words as the test items. In one block, the requirement was to respond positively to test items corresponding to studied words and to reject both new items and items corresponding to the studied pictures. In the other block, positive responses were made to test items corresponding to pictures, and items corresponding to words were classified along with the new items. On the basis of previous ERP findings, we predicted that in the word task, recollection-related effects would be found for target information only. This prediction was fulfilled. In both tasks, targets elicited the characteristic pattern of recollection-related activity. By contrast, nontargets elicited this pattern in the picture task, but not in the word task. Importantly, the left angular gyrus was among the regions demonstrating this dissociation of nontarget recollection effects according to retrieval orientation. The findings for the angular gyrus parallel prior findings for the "left-parietal" ERP old/new effect and add to the evidence that the effect reflects recollection-related neural activity originating in left ventral parietal cortex. Thus, the results converge with the previous ERP findings to suggest that the processing of retrieval cues can be constrained to prevent the retrieval of goal-irrelevant information.

Decoding episodic memory in ageing: a Bayesian analysis of activity patterns predicting memory.

Normal ageing is associated with a decline in episodic memory, and neuroimaging studies in older adults have shown reduced activity in prefrontal cortex and other regions critical for memory function in the young. However, older adults also activate additional regions, suggesting a degree of functional reorganisation that has been attributed variously to detrimental and adaptive changes. Evaluation of these competing hypotheses depends critically upon inferences about the relative location and distribution of activity that are not well supported by current univariate or multivariate analyses. Here, we employed a recently developed model-based multivariate 'decoding' approach (Friston et al., 2008) to re-analyse a rich episodic encoding dataset and examine directly how the patterns of activity change in ageing. We assessed which spatial activity patterns, within lateral prefrontal cortex, best predict successful memory formation. Bayesian model comparison showed that the older adults had more distributed and bilateral (fragmented) predictive patterns of activity in anterior inferior frontal gyrus and middle frontal gyrus. With this direct multivariate test for changes in patterns of activity, we replicate and extend earlier findings of reduced prefrontal lateralisation in ageing. These findings extend conclusions based on conventional analyses, and support the notion that ageing alters the spatial deployment of neuronal activity, to render it less spatially coherent and regionally specific. This greater distribution of activity in older adults was also linked to poorer individual memory performance, suggesting that it reflects neural ageing, rather than adaptive compensatory responses.

Memory encoding and dopamine in the aging brain: a psychopharmacological neuroimaging study.

Normal aging brings with it changes in dopaminergic and memory functions. However, little is known about how these 2 changes are related. In this study, we identify a link between dopamine, episodic memory networks, and aging, using pharmacological functional magnetic resonance imaging. Young and older adults received a D2-like agonist (Bromocriptine, 1.25 mg), a D2-like antagonist (Sulpiride, 400 mg), and Placebo, in a double-blind crossover procedure. We observed group differences, during memory encoding, in medial temporal, frontal, and striatal regions and moreover, these regions were differentially sensitive across groups to dopaminergic perturbation. These findings suggest that brain systems underlying memory show age-related changes and that dopaminergic function may be key in understanding these changes. That these changes have behavioral consequences was suggested by the observation that drug modulations were most pronounced in older subjects with poorer recognition memory. Our findings provide direct evidence linking ageing, memory, and dopaminergic change.