Using recognition testing to support semantic learning in developmental amnesia.

ABSTRACTPatients with developmental amnesia (DA) have suffered hippocampal damage in infancy and subsequently shown poor episodic memory, but good semantic memory. It is not clear how patients with DA learn semantic information in the presence of episodic amnesia. However, patients with DA show good recognition memory and it is possible that semantic learning may be supported by recognition. Building on previous work, we compared two methods for supporting semantic learning in DA; recognition-learning and recall-learning. In each condition, a patient with DA (aged 8 years) was presented with semantic information in animated videos. After each presentation of a video, learning was supported by an immediate memory test. Two videos were paired with a cued recall test. Another two videos were paired with a multiple-choice test to enable recognition-based learning. The outcome measure was semantic recall performance after a short delay of 30 min and a long delay of one week. Results showed a benefit of recognition-learning compared to recall-learning on cued recall in the patient with DA (76% vs. 35%). This finding indicates that young people with severe hippocampal damage can utilize recognition to support semantic learning. This has implications for the support of school-aged children with episodic memory difficulties.

Recollection-related increases in functional connectivity predict individual differences in memory accuracy.

Recollection involves retrieving specific contextual details about a prior event. Functional neuroimaging studies have identified several brain regions that are consistently more active during successful versus failed recollection-the "core recollection network." In the present study, we investigated whether these regions demonstrate recollection-related increases not only in activity but also in functional connectivity in healthy human adults. We used fMRI to compare time-series correlations during successful versus unsuccessful recollection in three separate experiments, each using a different operational definition of recollection. Across experiments, a broadly distributed set of regions consistently exhibited recollection-related increases in connectivity with different members of the core recollection network. Regions that demonstrated this effect included both recollection-sensitive regions and areas where activity did not vary as a function of recollection success. In addition, in all three experiments the magnitude of connectivity increases correlated across individuals with recollection accuracy in areas diffusely distributed throughout the brain. These findings suggest that enhanced functional interactions between distributed brain regions are a signature of successful recollection. In addition, these findings demonstrate that examining dynamic modulations in functional connectivity during episodic retrieval will likely provide valuable insight into neural mechanisms underlying individual differences in memory performance.

Motivated Memories: Effects of Reward and Recollection in the Core Recollection Network and Beyond.

fMRI was employed to assess whether the neural correlates of accurate source memory are modulated by the reward value of recollected information. Study items comprised pictures of objects, each paired with a depiction of 1 of 2 coins. The reward value of the coins ($2.00 vs. $0.02) was disclosed after study. At test, a source memory procedure was employed in which subjects discriminated between studied and unstudied objects and, for objects judged studied, indicated the identity of the coin paired with the object at study. Correct judgments earned a reward corresponding to the value of the coin, whereas incorrect judgments were penalized. No regions were identified where the magnitude of recollection effects was modulated by reward. Exclusive effects of source accuracy were evident in the hippocampus. Different striatal sub-regions demonstrated exclusive recollection effects, exclusive reward effects, and overlap between the 2 effects. The left angular gyrus and medial prefrontal cortex were additively responsive to source accuracy and the reward. The findings suggest that reward value and recollection success are conjointly but independently represented in at least 2 cortical regions and that striatal retrieval success effects cannot be accounted for in terms of a single construct, such as goal satisfaction.

Retrieval Goal Modulates Memory for Context.

fMRI was employed to assess whether the contents of recollection vary according to retrieval goal. At study, visually presented words were superimposed on urban or rural scenes or a gray background. The word-background pairs were presented in one of three spatial locations. During a scanned test phase, studied and unstudied words were presented. Two different source memory tasks were randomly interleaved. In the "background" task, the requirement was to judge whether the word had been presented against one of the two classes of scene, as opposed to the alternate class or the gray background. In the "location" task, discrimination was between words presented in one of the two lateral locations and words presented in either of the alternate locations. In both tasks, unstudied words required a separate response. In the background task, words studied against scenes elicited greater activity in parahippocampal and retrosplenial cortex than did words studied against the gray background, consistent with prior reports of scene reinstatement effects. Reinstatement effects were also evident in the location task. Relative to the background task, however, the effects were attenuated in parahippocampal cortex. In other regions, including medial prefrontal and posterior cingulate cortex, activity elicited in the location task by items associated with scenes was lower than that elicited by items presented on the gray background. The findings are interpreted as evidence that contextual retrieval is partially modulated by retrieval goal.

When the brain, but not the person, remembers: Cortical reinstatement is modulated by retrieval goal in developmental amnesia.

Developmental amnesia (DA) is associated with early hippocampal damage and subsequent episodic amnesia emerging in childhood alongside age-appropriate development of semantic knowledge. We employed fMRI to assess whether patients with DA show evidence of 'cortical reinstatement', a neural correlate of episodic memory, despite their amnesia. At study, 23 participants (5 patients) were presented with words overlaid on a scene or a scrambled image for later recognition. Scene reinstatement was indexed by scene memory effects (greater activity for previously presented words paired with a scene rather than scrambled images) that overlapped with scene perception effects. Patients with DA demonstrated scene reinstatement effects in the parahippocampal and retrosplenial cortex that were equivalent to those shown by healthy controls. Behaviourally, however, patients with DA showed markedly impaired scene memory. The data indicate that reinstatement can occur despite hippocampal damage, but that cortical reinstatement is insufficient to support accurate memory performance. Furthermore, scene reinstatement effects were diminished during a retrieval task in which scene information was not relevant for accurate responding, indicating that strategic mnemonic processes operate normally in DA. The data suggest that cortical reinstatement of trial-specific contextual information is decoupled from the experience of recollection in the presence of severe hippocampal atrophy.

Effects of age on goal-dependent modulation of episodic memory retrieval.

Retrieval gating refers to the ability to modulate the retrieval of features of a single memory episode according to behavioral goals. Recent findings demonstrate that younger adults engage retrieval gating by attenuating the representation of task-irrelevant features of an episode. Here, we examine whether retrieval gating varies with age. Younger and older adults incidentally encoded words superimposed over scenes or scrambled backgrounds that were displayed in one of three spatial locations. Participants subsequently underwent fMRI as they completed two memory tasks: the background task, which tested memory for the word's background, and the location task, testing memory for the word's location. Employing univariate and multivariate approaches, we demonstrated that younger, but not older adults, exhibited attenuated reinstatement of scene information when it was goal-irrelevant (during the location task). Additionally, in younger adults only, the strength of scene reinstatement in the parahippocampal place area during the background task was related to item and source memory performance. Together, these findings point to an age-related decline in the ability to engage retrieval gating.

Functional magnetic resonance imaging.

Among the range of methods available to assess neurodevelopmental disorders, functional MRI (fMRI) has been a preferred tool of choice. Indeed, fMRI can reveal functional alterations in brain networks, irrespective of their structural integrity. Yet, whether fMRI studies have provided unique added value and influenced the clinical care and assessments in children with these conditions remains controversial. This chapter aims to give an overview of the clinical use of task-based as well as resting-state fMRI in children with neurodevelopmental disorders, such as dyslexia, DLD, and epilepsy. We introduce analysis methods that appear promising (namely PPI and machine learning) and describe strengths and limitations of fMRI in the field of pediatrics. Altogether, we suggest that fMRI has provided us with a unique understanding of some developmental conditions. Indeed, findings from group studies have both informed neuroanatomical models and revealed compensation mechanisms. In addition, improvements have made fMRI an increasingly child-friendly method. Nevertheless, clinicians should be aware of limitations, including (1) lack of replication of results, (2) the limited specificity as a diagnostic tool, and (3) difficulties with interpretation of findings. The use of fMRI in the clinic currently remains restricted, with the exception of epilepsy surgery planning, where it is used routinely.

Neural correlates of individual differences in strategic retrieval processing.

Processes engaged when information is encoded into memory are an important determinant of whether that information will be recovered subsequently. Also influential, however, are processes engaged at the time of retrieval, and these were investigated here by using event-related potentials (ERPs) to measure a specific class of retrieval operations. These operations were revealed by contrasts between ERPs elicited by new (unstudied) test items in distinct tasks, the assumption being that these contrasts index operations that are engaged in service of retrieval and that vary according to the demands of different retrieval tasks. Specific functional accounts of this class of retrieval processing operations assume that they influence the accuracy of memory judgments, and this experiment was designed to test for the first time whether this is in fact the case. Toward this end, participants completed 2 retrieval tasks while ERPs were acquired, and the extent to which processes were engaged differentially across tasks in service of retrieval was operationalized as the magnitude of the differences between the new-item ERPs that were elicited. This measure correlated positively with response accuracy on the tasks, which provides strong evidence that this class of retrieval processing operations benefits the accuracy of memory judgments.

Little evidence for fast mapping in adults with developmental amnesia.

Cooper, Greve, and Henson (this issue) conclude that hippocampal-independent learning, as operationalised by 'fast mapping' (FM), is unlikely to facilitate learning in adults. We provide evidence from patients with Developmental Amnesia (DA), who acquire language and semantic knowledge despite early hippocampal pathology. We administered an FM paradigm to three patients with DA and controls. Patients showed no benefit of FM compared to explicit encoding. These data support the conclusion that FM is unlikely to facilitate learning in amnesia, regardless of age at onset. Hippocampal-independent learning may be possible in adults with DA, but such learning requires a prolonged consolidation period.

Semantic memory in developmental amnesia.

Patients with developmental amnesia resulting from bilateral hippocampal atrophy associated with neonatal hypoxia-ischaemia typically show relatively preserved semantic memory and factual knowledge about the natural world despite severe impairments in episodic memory. Understanding the neural and mnemonic processes that enable this context-free semantic knowledge to be acquired throughout development without the support of the contextualised episodic memory system is a serious challenge. This review describes the clinical presentation of patients with developmental amnesia, contrasts its features with those reported for adult-onset hippocampal amnesia, and analyses the effects of variables that influence the learning of new semantic information.

Dissociation between the neural correlates of recollection and familiarity in the striatum and hippocampus: Across-study convergence.

In tests of recognition memory, neural activity in the striatum has consistently been reported to differ according to the study status of the test item. A full understanding of the functional significance of striatal 'retrieval success' effects is impeded by a paucity of evidence concerning whether the effects differ according to the nature of the memory signal supporting the recognition judgment (recollection vs. familiarity). Here, we address this issue through an analysis of retrieval-related striatal activity in three independent fMRI studies (total N = 88). Recollection and familiarity were operationalized in a different way in each study, allowing the identification of test-independent, generic recollection- and familiarity-related effects. While activity in a bilateral dorsal striatal region, mainly encompassing the caudate nucleus, was enhanced equally by recollected and 'familiar only' test items, activity in bilateral ventral striatum and adjacent subgenual frontal cortex was enhanced only in response to items that elicited successful recollection. By contrast, relative to familiar items, activity in anterior hippocampus was enhanced for both recollected and novel test items. Thus, recollection- and familiarity-driven recognition memory judgments are associated with anatomically distinct patterns of retrieval-related striatal activity, and these patterns are at least partially independent of recollection and novelty effects in the hippocampus.

Reduced specificity of autobiographical memory and depression: the role of executive control.

It has been widely established that depressed mood states and clinical depression, as well as a range of other psychiatric disorders, are associated with a relative difficulty in accessing specific autobiographical information in response to emotion-related cue words on an Autobiographical Memory Test (AMT; J. M. G. Williams & K. Broadbent, 1986). In 8 studies the authors examined the extent to which this relationship is a function of impaired executive control associated with these mood states and clinical disorders. Studies 1-4 demonstrated that performance on the AMT is associated with performance on measures of executive control, independent of depressed mood. Furthermore, Study 1 showed that executive control (as measured by verbal fluency) mediated the relationship between both depressed mood and a clinical diagnosis of eating disorder and AMT performance. Using a stratified sample in Study 5, the authors confirmed the positive association between depressed mood and impaired performance on the AMT. Studies 6-8 involved experimental manipulations of the parameters of the AMT designed to further indicate that reduced executive control is to a significant extent driving the relationship between depressed mood and AMT performance. The potential role of executive control in accounting for other aspects of the AMT literature is discussed.

The role of working memory capacity in the control of recollection.

The links between control over recollection and working memory capacity (WMC) were investigated using event-related potentials (ERPs) and behavioural assays. Electrophysiological evidence for a relationship between greater control over recollection and higher scores on a measure of WMC was obtained. In addition, people with high WMC who first completed a task requiring cognitive control showed no electrophysiological evidence for control over recollection on a subsequent task. This outcome suggests a causal link between control over recollection and the availability of WMC, in so far as the consequence of completing the first task was a reduction in WMC that impacted on completion of the subsequent task. All participants also completed a final recall task, on which they were asked to remember the stimuli they had encountered during the task in which ERPs were acquired. Only those participants who showed electrophysiological evidence for the exertion of control over recollection showed differences between the likelihoods of recalling stimuli over which control either had or had not been exerted. In combination, the findings provide insights into the conditions under which control over recollection occurs, and make a strong argument for including individual difference measures of resource availability when assessing how and when people exert control over what they remember.

Cross-modal face identity aftereffects and their relation to priming.

We tested the magnitude of the face identity aftereffect following adaptation to different modes of adaptors in four experiments. The perceptual midpoint between two morphed famous faces was measured pre- and post-adaptation. Significant aftereffects were observed for visual (faces) and nonvisual adaptors (voices and names) but not nonspecific semantic information (e.g., occupations). Aftereffects were also observed following imagination and adaptation to an associated person. The strongest aftereffects were found adapting to facial caricatures. These results are discussed in terms of cross-modal adaptation occurring at various loci within the face-recognition system analogous to priming.

Identity adaptation is mediated and moderated by visualisation ability.

Depending on the previous research one reads, face aftereffects may or may not partially transfer across viewpoints. Two experiments are reported that explore this face-identity aftereffect by varying the adaptor type. Adaptation occurs when different views of the identity are used and even when the person's name is the adaptor. Brief exposure or nationality did not produce adaptation. In a third experiment, the role of visualisation was explored. Participants with higher visualisation scores showed greater adaptation to names than those with lower scores. These findings suggest non-facial identity cues can lead to a facial adaptation effect and that visualisation may be the mechanism behind this.