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1.  Lateral parietal cortex is modulated by amount of recollected verbal information 
Neuroreport  2009;20(14):1295-1299.
In two prior experiments we reported that activity in the left inferior posterior parietal cortex covaried with amount of information recollected. Given that the experimental materials in these two studies were exclusively pictorial, the question arises whether the findings generalize to other classes of recollected content. If, as we have argued, the left inferior parietal cortex supports the representation of recollected content in an amodal manner, then activity in this region should also be modulated by amount recollected when non-pictorial materials are employed. The current study addressed the question whether left inferior posterior parietal cortex is sensitive to amount of information recollected for verbal rather than pictorial information. At study, participants saw a series of word pairs, in each case generating a sentence that incorporated both words. At test, a mixture of old and new individual words were presented in a modified remember/know task. Participants made one response (R2) if they could recollect the test item and its studied pairmate, another response (R1) if they could recollect some information from the study episode but not the pairmate, a third response (K) if the test item was judged to have been studied in the absence of any recollection of study details, or a fourth, New, response. We assumed that trials where old items were given an R2 response were on average associated with recollection of more study information than when old items were given an R1 response. Thus, we operationally defined ‘amount recollected’ as the contrast between these two trial types (i.e., R2 hits > R1 hits). Using a small volume correction procedure, we identified a cluster within the same left inferior posterior parietal region identified as amount-sensitive in our prior study using the same test procedure. Thus, our prior findings generalize to non-pictorial stimulus materials and support the proposal that left inferior posterior parietal cortex plays a generic role in the maintenance or representation of recollected information.
PMCID: PMC2771458  PMID: 19668014
episodic memory; remember-know; recollection
2.  Sleep-Related Hippocampo-Cortical Interplay during Emotional Memory Recollection 
PLoS Biology  2007;5(11):e282.
Emotional events are usually better remembered than neutral ones. This effect is mediated in part by a modulation of the hippocampus by the amygdala. Sleep plays a role in the consolidation of declarative memory. We examined the impact of sleep and lack of sleep on the consolidation of emotional (negative and positive) memories at the macroscopic systems level. Using functional MRI (fMRI), we compared the neural correlates of successful recollection by humans of emotional and neutral stimuli, 72 h after encoding, with or without total sleep deprivation during the first post-encoding night. In contrast to recollection of neutral and positive stimuli, which was deteriorated by sleep deprivation, similar recollection levels were achieved for negative stimuli in both groups. Successful recollection of emotional stimuli elicited larger responses in the hippocampus and various cortical areas, including the medial prefrontal cortex, in the sleep group than in the sleep deprived group. This effect was consistent across subjects for negative items but depended linearly on individual memory performance for positive items. In addition, the hippocampus and medial prefrontal cortex were functionally more connected during recollection of either negative or positive than neutral items, and more so in sleeping than in sleep-deprived subjects. In the sleep-deprived group, recollection of negative items elicited larger responses in the amygdala and an occipital area than in the sleep group. In contrast, no such difference in brain responses between groups was associated with recollection of positive stimuli. The results suggest that the emotional significance of memories influences their sleep-dependent systems-level consolidation. The recruitment of hippocampo-neocortical networks during recollection is enhanced after sleep and is hindered by sleep deprivation. After sleep deprivation, recollection of negative, potentially dangerous, memories recruits an alternate amygdalo-cortical network, which would keep track of emotional information despite sleep deprivation.
Author Summary
Declarative memories, which can be consciously and verbally retrieved, are initially critically dependent on the hippocampus. However, reliable retrieval of long-term memory depends on a process of consolidation, which partly occurs during sleep, when memories are thought to be progressively transferred to long-term cortical stores. Because people tend to remember emotional memories better than neutral ones, we wondered whether the emotional significance of a memory would enhance its consolidation in a sleep-dependent manner. During a first session, participants viewed pictures with neutral and emotional content without realizing that their memory of the pictures and their content would be tested later (called incidental encoding). Three days later, during a functional MRI scanning session, subjects indicated whether they recognized previously viewed and new pictures. Half of the subjects were totally sleep deprived during the first post-encoding night, but all subjects slept as usual during the second and third post-encoding nights. We show here that the recollection of emotional stimuli elicited larger responses in the hippocampus and various cortical areas in the well-rested group than in the sleep-deprived group, suggesting that emotional significance boosts memory consolidation of the information during sleep. Interestingly, in sleep-deprived subjects, recollection of negative items recruited another network including the amygdala, as if an alternate consolidation process allowed them to keep track of negative, potentially dangerous, information despite the cognitive aftermath of sleep deprivation.
A new fMRI study reveals that emotional memories are consolidated by different brain networks in humans who receive a normal amount of sleep, compared with those who are sleep deprived.
PMCID: PMC2039770  PMID: 17958471
Depression and anxiety  2009;26(5):396-402.
The memory deficit hypothesis has been used to explain the maintenance of repetitive behavior in individuals with obsessive–compulsive disorder, yet the majority of studies focusing on verbal memory show mixed results. These studies primarily evaluated memory accuracy via the inclusion or omission of previously encountered material, as opposed to false recognition (i.e., the inclusion of erroneous material). We evaluated false memories and memory processes in individuals with obsessive–compulsive washing symptoms (OC), individuals matched on depression and anxiety without OC symptoms (D/A), and in nonanxious individuals (NAC).
Twenty-eight OC, 28 D/A, and 29 NAC individuals read OC-threat relevant, positive, and neutral scenarios and then performed a recognition test. Erroneous recognition of words associated to encoded, but not previously viewed, scenarios were classified as false memories. To evaluate processes underlying memory, participants completed a modified remember/know task to examine whether the OC individuals differed from the other individuals in recollective clarity for false memories of OC-relevant (e.g., germs), positive (e.g., lottery), and neutral (e.g., bread) material.
The OC individuals used “know” more than the D/A and NAC individuals for false memories of threat. For veridical memories, the OC individuals used “know” more than the NAC, but not, D/A individuals.
The greater reliance on “know” (i.e., feelings of familiarity) in general and false threat memories in particular in individuals with OC symptoms may add to feelings of uncertainty for threat-relevant material, which may contribute to compulsive behavior.
PMCID: PMC3666829  PMID: 18839404
Threat; Recognition; Deficit; Remember; Know
4.  True Memory, False Memory, and Subjective Recollection Deficits after Focal Parietal Lobe Lesions 
Neuropsychology  2010;24(4):465-475.
There is mounting evidence that the posterior parietal cortex (PPC) plays an important role in episodic memory. We previously found that patients with PPC damage exhibit retrieval-related episodic memory deficits. Our objective was to assess whether parietal lobe damage affects episodic memory on a different task: the Deese-Roediger-McDermott (DRM) false-memory paradigm.
Two patients with bilateral PPC damage and matched controls were tested. In Experiment 1, the task was to remember words; in Experiment 2 the task was to remember pictures of common objects. Prior studies have shown that normal participants have high levels of false memory to words, low levels to pictures.
The patients exhibited significantly lower levels of false memory to words. The patients' false memories were accompanied by reduced levels of recollection, as tested by a Remember/Know procedure. It is unlikely that a failure of gist processing accounts for these results, as patients accurately remembered thematic elements of short vignettes, but failed to remember details. These results support the view that portions of the PPC play a critical role in objective and subjective aspects of recollection.
PMCID: PMC2917642  PMID: 20604621
false memory; subjective recollection; attention; parietal lobe; memory retrieval; Balint's syndrome; simultanagnosia
5.  Remember and Know Judgments During Recognition in Chronic Schizophrenia 
Schizophrenia research  2007;100(1-3):181-190.
Deficits in learning and memory are among the most robust correlates of schizophrenia. It has been hypothesized that these deficits are in part due to reduced conscious recollection and increased reliance on familiarity assessment as a basis for retrieval. The Remember-Know (R-K) paradigm was administered to 35 patients with chronic schizophrenia and 35 healthy controls. In addition to making “remember” and “know” judgments, the participants were asked to make forced choice recognition judgments with regard to details about the learning episode. Analyses comparing response types showed a significant reduction in “remember” responses and a significant increase in “know” responses in schizophrenia patients relative to controls. Both patients and controls recalled more details of the learning episode for “remember” compared to “know” responses, although, in particular for “remember” responses, patients recalled fewer details compared with controls. Notably, patients recognized fewer inter-item but not intra-item stimulus features compared with controls. These findings suggest deficits in organizing and integrating relational information during the learning episode and/or using relational information for retrieval. A Dual-Process Signal Detection interpretation of these findings suggests that recollection in chronic schizophrenia is significantly reduced, while familiarity is not. Additionally, a unidimensional Signal Detection Theory interpretation suggests that chronic schizophrenia patients show a reduction in memory strength, and an altered criterion on the memory strength distribution for detecting new compared with old stimuli but not for detecting stimuli that are remembered versus familiar. Taken together, these findings are consistent with a deficit in recollection and increased reliance on familiarity in making recognition memory judgments in chronic schizophrenia.
PMCID: PMC2517628  PMID: 17964760
schizophrenia; psychosis; chronic; memory; episodic; recognition; recollection; familiarity; context; remember; know
6.  Dissociation of the neural correlates of recognition memory according to familiarity, recollection, and amount of recollected information 
Neuropsychologia  2007;45(10):2216-2225.
The present experiment used fMRI to investigate whether neural correlates of recognition memory behave in a manner consistent with the proposal that recognition decisions are based on a unidimensional memory strength variable. A modified remember/know recognition test was used in which participants could indicate two levels of recollection. Participants were required to indicate whether a test item was new, familiar (known), elicited recollection of general contextual details from the study episode (R1 response), or elicited a specific recollection of the item with which it was paired at study (R2 response). Little evidence could be found to support the view that Remember/Know/New judgments reflect variations along a single strength dimension. Instead, the findings replicated prior research in indicating that the neural correlates of recollection and familiarity can be doubly dissociated. Two recollection-sensitive regions - left lateral inferior parietal and left fusiform cortex - were found to be sensitive to amount of information recollected, as operationalized in the contrast between R2 and R1 responses. It is proposed that these regions may support the representation of recollected information.
PMCID: PMC1933497  PMID: 17449068
memory strength; fMRI; parietal; hippocampus; dual-process; brain imaging
7.  Relating the Content and Confidence of Recognition Judgments 
The Remember/Know procedure, developed by Tulving (1985) to capture the distinction between the conscious correlates of episodic and semantic retrieval, has spurned considerable research and debate. However, only a handful of reports have examined the recognition content beyond this dichotomous simplification. To address this, we collected participants’ written justifications in support of ordinary old/new recognition decisions accompanied by confidence ratings using a 3-point scale (high/medium/low). Unlike prior research, we did not provide the participants with any descriptions of Remembering or Knowing and thus, if the justifications mapped well onto theory, they would do so spontaneously. Word frequency analysis (unigrams, bigrams, and trigrams), independent ratings, and machine learning techniques (Support Vector Machine - SVM) converged in demonstrating that the linguistic content of high and medium confidence recognition differs in a manner consistent with dual process theories of recognition. For example, the use of ‘I remember’, particularly when combined with temporal or perceptual information (e.g., ‘when’, ‘saw’, ‘distinctly’), was heavily associated with high confidence recognition. Conversely, participants also used the absence of remembering for personally distinctive materials as support for high confidence new reports (‘would have remembered’). Thus, participants afford a special status to the presence or absence of remembering and use this actively as a basis for high confidence during recognition judgments. Additionally, the pattern of classification successes and failures of a SVM was well anticipated by the Dual Process Signal Detection model of recognition and inconsistent with a single process, strictly unidimensional approach. “One might think that memory should have something to do with remembering, and remembering is a conscious experience.”(Tulving, 1985, p. 1)
PMCID: PMC4049202  PMID: 23957366
8.  Functional Significance of Retrieval-related Activity in Lateral parietal cortex: Evidence from fMRI and ERPs 
Human brain mapping  2009;30(5):1490-1501.
The present study addressed the question whether neural activity in left lateral parietal cortex is modulated by amount of information recollected. In two experiments (one using fMRI, the other ERPs) subjects first studied pairs of pictures presented for either one or six seconds. They then performed a standard ‘Remember/Know’ recognition memory test in which the old items comprised one of the pictures from each studied pair. In both experiments, a surprise post-test indicated that subjects recollected more details about the study presentation of the items presented for the longer duration. In the fMRI experiment, recollection- and familiarity-based recognition elicited activity in distinct cortical networks. Additionally, recollection-related activity in left inferior parietal cortex was of greater magnitude for test items presented for six seconds than for one second. In the ERP study the ‘left-parietal old/new effect’ – a putative correlate of successful recollection – was likewise modulated by amount of information retrieved. Together, these findings provide further support for dual-process models of recognition memory and add weight to the proposal that retrieval-related activity in left inferior parietal cortex reflects processes supporting the online representation of retrieved episodic information.
PMCID: PMC2670940  PMID: 18649352
episodic memory; recognition memory; remember-know; event-related potential; episodic buffer
9.  Rethinking Familiarity: Remember/Know Judgments in Free Recall 
Journal of memory and language  2013;68(4):333-349.
Although frequently used with recognition, a few studies have used the Remember/Know procedure with free recall. In each case, participants gave Know judgments to a significant number of recalled items (items that were presumably not remembered on the basis of familiarity). What do these Know judgments mean? We investigated this issue using a source memory/free-recall procedure. For each word that was recalled, participants were asked to (a) make a confidence rating on a 5-point scale, (b) make a Remember/Know judgment, and (c) recollect a source detail. The large majority of both Remember judgments and Know judgments were made with high confidence and high accuracy, but source memory was nevertheless higher for Remember judgments than for Know judgments. These source memory results correspond to what is found using recognition, and they raise the possibility that Know judgments in free recall identify the cue-dependent retrieval of item-only information from an episodic memory search set. In agreement with this idea, we also found that the temporal dynamics of free recall were similar for high-confidence Remember and high-confidence Know judgments (as if both judgments reflected retrieval from the same search set). If Know judgments in free recall do in fact reflect the episodic retrieval of item-only information, it seems reasonable to suppose that the same might be true of high-confidence Know judgments in recognition. If so, then a longstanding debate about the role of the hippocampus in recollection and familiarity may have a natural resolution.
PMCID: PMC3637981  PMID: 23637470
Recollection; Familiarity; Recall; Recognition
10.  Memory for time and place contributes to enhanced confidence in memories for emotional events 
Emotion (Washington, D.C.)  2012;12(4):834-846.
Emotion strengthens the subjective sense of remembering. However, these confidently remembered emotional memories have not been found be more accurate for some types of contextual details. We investigated whether the subjective sense of recollecting negative stimuli is coupled with enhanced memory accuracy for three specific types of central contextual details using the remember/know paradigm and confidence ratings. Our results indicate that the subjective sense of remembering is indeed coupled with better recollection of spatial location and temporal context. In contrast, we found a double-dissociation between the subjective sense of remembering and memory accuracy for colored dots placed in the conceptual center of negative and neutral scenes. These findings show that the enhanced subjective recollective experience for negative stimuli reliably indicates objective recollection for spatial location and temporal context, but not for other types of details, whereas for neutral stimuli, the subjective sense of remembering is coupled with all the types of details assessed. Translating this finding to flashbulb memories, we found that, over time, more participants correctly remembered the location where they learned about the terrorist attacks on 9/11 than any other canonical feature. Likewise participants’ confidence was higher in their memory for location vs. other canonical features. These findings indicate that the strong recollective experience of a negative event corresponds to an accurate memory for some kinds of contextual details, but not other kinds. This discrepancy provides further evidence that the subjective sense of remembering negative events is driven by a different mechanism than the subjective sense of remembering neutral events.
PMCID: PMC3968901  PMID: 22642353
emotion; memory; subjective sense of remembering; remember/know; confidence
11.  Recognition memory in developmental prosopagnosia: electrophysiological evidence for abnormal routes to face recognition 
Dual process models of recognition memory propose two distinct routes for recognizing a face: recollection and familiarity. Recollection is characterized by the remembering of some contextual detail from a previous encounter with a face whereas familiarity is the feeling of finding a face familiar without any contextual details. The Remember/Know (R/K) paradigm is thought to index the relative contributions of recollection and familiarity to recognition performance. Despite researchers measuring face recognition deficits in developmental prosopagnosia (DP) through a variety of methods, none have considered the distinct contributions of recollection and familiarity to recognition performance. The present study examined recognition memory for faces in eight individuals with DP and a group of controls using an R/K paradigm while recording electroencephalogram (EEG) data at the scalp. Those with DP were found to produce fewer correct “remember” responses and more false alarms than controls. EEG results showed that posterior “remember” old/new effects were delayed and restricted to the right posterior (RP) area in those with DP in comparison to the controls. A posterior “know” old/new effect commonly associated with familiarity for faces was only present in the controls whereas individuals with DP exhibited a frontal “know” old/new effect commonly associated with words, objects and pictures. These results suggest that individuals with DP do not utilize normal face-specific routes when making face recognition judgments but instead process faces using a pathway more commonly associated with objects.
PMCID: PMC4132483  PMID: 25177283
prosopagnosia; face recognition; recognition memory; familiarity; recollection; electroencephalogram (EEG)
12.  Neural Substrates of Increased Memory Sensitivity for Negative Stimuli in Major Depression 
Biological psychiatry  2008;63(12):1155-1162.
Although memory biases for negatively valenced stimuli have been reliably associated with depression and have been postulated to play a critical role in the maintenance of this disorder, the neural bases of these biases have received little attention. In this study, we tested a model of heightened memory sensitivity for negative information in depression in which neural mechanisms that normally facilitate memory for affective material are over-recruited during encoding of negative material in depression.
We used functional magnetic resonance imaging to examine amygdala activity and functional connectivity with the hippocampus and caudate-putamen during successful encoding—as assessed by a recognition memory probe one week following scanning—of negative, neutral, and positive pictures by 14 depressed and 12 nondepressed individuals.
Depressed individuals demonstrated greater memory sensitivity than did nondepressed participants to negative, but not to neutral or positive, stimuli. The right amygdala was more active and showed greater functional connectivity with the hippocampus and caudate-putamen during encoding of subsequently remembered negative, but not neutral or positive, stimuli in depressed than in control participants. The degree of memory-related right amygdala responsivity in the depressed participants was significantly correlated with depressive severity.
These findings support the formulation that, in remembering negative information better than nondepressed persons, depressed individuals over-recruit a neural network involved more generally in enhancing memory for affective stimuli, and that the degree to which they over-recruit this system is related to the severity of clinical symptomatology.
PMCID: PMC2474758  PMID: 18281017
Depression; Amygdala; Hippocampus; Caudate; Putamen; Memory
13.  Aging reduces veridical remembering but increases false remembering: Neuropsychological test correlates of remember–know judgments 
Neuropsychologia  2008;47(11):2164-2173.
In 1985 Tulving introduced the remember–know procedure, whereby subjects are asked to distinguish between memories that involve retrieval of contextual details (remembering) and memories that do not (knowing). Several studies have been reported showing age-related declines in remember hits, which has typically been interpreted as supporting dual-process theories of cognitive aging that align remembering with a recollection process and knowing with a familiarity process. Less attention has been paid to remember false alarms, or their relation to age. We reviewed the literature examining aging and remember/know judgments and show that age-related increases in remember false alarms, i.e., false remembering, are as reliable as age-related decreases in remember hits, i.e., veridical remembering. Moreover, a meta-analysis showed that the age effect size for remember hits and false alarms are similar, and larger than age effects on know hits and false alarms. We also show that the neuropsychological correlates of remember hits and false alarms differ. Neuropsychological tests of medial-temporal lobe functioning were related to remember hits, but tests of frontal-lobe functioning and age were not. By contrast, age and frontal-lobe functioning predicted unique variance in remember false alarms, but MTL functioning did not. We discuss various explanations for these findings and conclude that any comprehensive explanation of recollective experience will need to account for the processes underlying both remember hits and false alarms.
PMCID: PMC3319377  PMID: 19100756
Human memory; Episodic memory; Cognitive aging; Remember–know; Meta-analysis; Frontal functioning; Medial-temporal functioning; Signal detection
14.  Face Memory: Implications for theories of binding items to context 
Psychological science  2013;24(3):363-372.
Two experiments tested the hypothesis that it is easier to bind a stimulus to context when the stimulus already has a stable (i.e., pre-existing) memory representation by comparing episodic memory of faces of celebrities vs. unknown individuals. Each face was superimposed on a picture of a well-known location (e.g., Eiffel Tower) during encoding and at a later unexpected recognition test but the background could change from encoding to test. Although recognition was to be based on the face, irrespective of background, performance was better when encoding context was reinstated. Further, a given background could be shown with many faces ("high fan") or only a few ("low fan") and this variable modulated the value added of context reinstatement. Importantly, manipulations of context only mattered for famous faces. As predicted, these effects were observed in recollection ("Remember") responses not in familiarity (“Know”) responses. Experiment 2 used the same design except that half of the subjects were administered midazolam, a drug that produces temporary anterograde amnesia, prior to encoding faces and backgrounds. Subjects injected with saline (control condition) showed the same pattern as Experiment 1; however subjects injected with midazolam showed a large decrease in the use of the "Remember" responses for famous faces and neither context reinstatement nor background fan affected performance. These results support the view that it is easier to bind stimuli to context when stimuli have a pre-existing, stable memory representation (e.g., faces of people whose identity we know) than when stimuli do not have pre-existing, stable memory representations.
PMCID: PMC4180115  PMID: 23395827
Recollection; familiarity; binding; memory; amnesia; faces; context
15.  Episodic memory in schizophrenia: The influence of strategy use on behavior and brain activation 
Psychiatry research  2008;164(1):1-15.
Individuals with schizophrenia demonstrate behavioral and neurobiological deficits in episodic memory. However, recent work suggests that episodic memory deficits in schizophrenia may be mitigated through specific encoding strategies. The current study directly compared brain activity and memory performance associated with two different verbal encoding orientations in the same group of schizophrenia participants, in order to more fully characterize the role of strategy in memory processing in this population. Participants included 18 individuals with schizophrenia and 15 healthy comparison participants. Participants encoded words under two conditions during separate fMRI scanning runs. During Incidental encoding, participants were required to make abstract/concrete judgments for each word. During Intentional encoding, participants were instructed to memorize each word for a later memory test. Free recall and a recognition task (utilizing the Remember/Know paradigm) were performed outside of the scanner. Consistent with prior work, schizophrenia participants recognized more words encoded Incidentally than Intentionally, although free recall remained substantially impaired. Schizophrenia participants were also less likely to give Remember judgments for old words and more likely to give Guess judgments for both old and new words. When fMRI data were examined, we found that Incidental encoding was associated with substantially fewer between-group differences (Control > Schizophrenia) than Intentional encoding. Furthermore, schizophrenia participants exhibited intact activity during encoding of items that were subsequently retrieved. Our results suggest that use of an Incidental encoding strategy improved recognition memory among individuals with schizophrenia and resulted in a pattern of encoding-related brain activity that was more similar to that seen in control participants. However, we found that Incidental encoding did not improve free recall in schizophrenia participants and abnormal brain activity in some regions was observed, despite improvements in recognition memory.
PMCID: PMC2659741  PMID: 18790618
functional magnetic resonance imaging (fMRI); subsequent memory; incidental encoding
16.  Changes in Familiarity and Recollection across the Lifespan: An ERP Perspective 
Brain research  2009;1310C:124-141.
The ability to recognize previous experience depends on two neurocognitive processes, familiarity, fast-acting and relatively automatic, and recollection, slower-acting and more effortful. Familiarity appears to mature relatively early in development and is maintained with aging, whereas recollection shows protracted development and deteriorates with aging. To assess this model, ERP and behavioral data were recorded in children (9-10 years), adolescents (13-14), young (20-30) and older (65-85) adults during a recognition memory task in which the same items were studied and tested over four cycles. Participants decided whether each item was old or new and then whether the decision was associated with (Remember, R) or without (Know, K) contextual detail. Memory sensitivity was greatest in young adults, although all groups showed increases in memory sensitivity and R judgments with repetition. Familiarity-based processes (mid-frontal episodic memory, EM, effect) appeared to be used by adolescents, young and older adults, but apparently not to the same extent by children. Recollection-based processes (parietal EM effect) were recruited by children, adolescents and young adults, but to a much lesser extent by older adults. Repetition enhanced the parietal effect in all but older adults. However, post-hoc analyses indicated that reduced recollective processing was confined to poor-performing older adults. By contrast, children appeared to rely mainly on recollection concordant with their conservative decision criteria across tests. We conclude that episodic-memory development reflects the increasingly flexible and interchangeable use of familiarity and recollection with a breakdown in the latter at older ages, perhaps limited to poor-performing older adults.
PMCID: PMC2812671  PMID: 19914220
ERP episodic memory effect; lifespan; cognitive development; cognitive aging; familiarity; recollection
17.  Perceptual salience affects the contents of working memory during free-recollection of objects from natural scenes 
One of the most important issues in the study of cognition is to understand which are the factors determining internal representation of the external world. Previous literature has started to highlight the impact of low-level sensory features (indexed by saliency-maps) in driving attention selection, hence increasing the probability for objects presented in complex and natural scenes to be successfully encoded into working memory (WM) and then correctly remembered. Here we asked whether the probability of retrieving high-saliency objects modulates the overall contents of WM, by decreasing the probability of retrieving other, lower-saliency objects. We presented pictures of natural scenes for 4 s. After a retention period of 8 s, we asked participants to verbally report as many objects/details as possible of the previous scenes. We then computed how many times the objects located at either the peak of maximal or minimal saliency in the scene (as indexed by a saliency-map; Itti et al., 1998) were recollected by participants. Results showed that maximal-saliency objects were recollected more often and earlier in the stream of successfully reported items than minimal-saliency objects. This indicates that bottom-up sensory salience increases the recollection probability and facilitates the access to memory representation at retrieval, respectively. Moreover, recollection of the maximal- (but not the minimal-) saliency objects predicted the overall amount of successfully recollected objects: The higher the probability of having successfully reported the most-salient object in the scene, the lower the amount of recollected objects. These findings highlight that bottom-up sensory saliency modulates the current contents of WM during recollection of objects from natural scenes, most likely by reducing available resources to encode and then retrieve other (lower saliency) objects.
PMCID: PMC4330792  PMID: 25741266
visual; salience; working memory; capacity; free recollection; objects; natural scenes
18.  Medial prefrontal cortex activity during memory encoding of pictures and its relation to symptomatic improvement after citalopram treatment in patients with major depression 
Brain imaging studies of major depressive disorder have shown alterations in the brain regions typically involved in episodic memory, including the prefrontal cortex and medial temporal areas. Some studies of major depressive disorder have linked episodic memory performance to treatment response. In this study, we sought to identify brain regions whose activity, measured during the encoding of pictures, predicted symptomatic improvement after 8 weeks of citalopram treatment.
We included 20 unmedicated depressed patients. These patients performed an episodic recognition memory task during functional magnetic resonance imaging. During the encoding phase, 150 pictures depicting emotionally positive, negative or neutral content were presented, and the participants were required to classify each picture according to its emotional valence. The same 150 pictures were presented, along with 150 new ones, for a recognition task. We asked participants to distinguish the old pictures from the new ones. We assessed symptom severity by use of the 21-item Hamilton Rating Scale for Depression (HAM-D) at baseline and after 8 weeks of citalopram treatment. We performed subsequent memory effect analyses using SPM2 software. We explored the relation between brain activation during successful encoding of pictures and symptomatic improvement.
Patients showed a mean symptomatic improvement of 54.5% on the HAM-D after 8 weeks. Symptomatic improvement was significantly and positively correlated with picture recognition memory accuracy. We also found that the activity of the ventromedial prefrontal cortex and anterior cingulate cortex during successful encoding was significantly correlated with symptomatic improvement. Finally, we found greater activation in the ventromedial prefrontal cortex during the successful encoding of positive pictures in comparison with neutral pictures.
During the recognition memory task, 5 participants (among the best responders to treatment) were not included in the valence-specific analyses because they had very few errors. A more challenging task would have allowed the inclusion of most patients.
Different types of functional imaging paradigms have been used to explore whether the activity of specific brain regions measured at baseline is predictive of a better response to treatment in major depressive disorder. Among these regions, the medial prefrontal cortex and anterior cingulate cortex usually show the strongest predictive value. According to our results, the medial prefrontal cortex and anterior cingulate cortex could have an effect on treatment response in major depressive disorder by contributing to the successful encoding of positively valenced information.
PMCID: PMC2861132  PMID: 20420766
19.  Prior perceptual processing enhances the effect of emotional arousal on the neural correlates of memory retrieval 
A fundamental idea in memory research is that items are more likely to be remembered if encoded with a semantic, rather than perceptual, processing strategy. Interestingly, this effect has been shown to reverse for emotionally arousing materials, such that perceptual processing enhances memory for emotional information or events. The current fMRI study investigated the neural mechanisms of this effect by testing how neural activations during emotional memory retrieval are influenced by the prior encoding strategy. Participants incidentally encoded emotional and neutral pictures under instructions to attend to either semantic or perceptual properties of each picture. Recognition memory was tested two days later. fMRI analyses yielded three main findings. First, right amygdalar activity associated with emotional memory strength was enhanced by prior perceptual processing. Second, prior perceptual processing of emotional pictures produced a stronger effect on recollection- than familiarity-related activations in the right amygdala and left hippocampus. Finally, prior perceptual processing enhanced amygdalar connectivity with regions strongly associated with retrieval success, including hippocampal/parahippocampal regions, visual cortex, and ventral parietal cortex. Taken together, the results specify how encoding orientations yield alterations in brain systems that retrieve emotional memories.
PMCID: PMC4051848  PMID: 24380867
Emotion; Memory; Amygdala; fMRI
20.  Behavioral and neural evidence for masked conceptual priming of recollection 
Previous research has found that masked repetition primes, presented immediately prior to the test item in a recognition memory test, increase the likelihood that participants think that the item was present in a previous study phase, even if it was not. This memory illusion is normally associated with a feeling of familiarity, rather than recollection (e.g., as indexed by Remember/Know judgments), and has been explained in terms of an increased fluency of processing the test item, which, in the absence of awareness of the cause of that fluency (i.e., the masked prime), is attributed instead to prior exposure in the study phase. Recently however, we have found that masked conceptual primes (semantically rather than associatively related to the test item) have the opposite effect of increasing Remember but not Know judgments. This result appears difficult to explain in terms of existing theories of recollection and familiarity. Here we report data from a functional magnetic resonance imaging study using the same design, in which we replicate our previous behavioral findings, and find converging evidence for increased activity following conceptual primes in brain regions associated with recollection. This neural evidence supports an account in terms of “true” recollection (for example, conceptual primes reactivating semantically related information that was generated at encoding), rather than an artifact of the mutually-exclusive nature of the Remember/Know procedure.
PMCID: PMC3690477  PMID: 23026757
Recollection; Familiarity; fMRI; Conceptual priming; Repetition priming
21.  SenseCam, imagery and bias in memory for wellbeing 
Memory (Hove, England)  2011;19(7):768-777.
Identifying and modifying the negative interpretation bias that characterises depression is central to successful treatment. While accumulating evidence indicates that mental imagery is particularly effective in the modification of emotional bias, this research typically incorporates static and unrelated ambiguous stimuli. SenseCam technology, and the resulting video-like footage, offers an opportunity to produce training stimuli that are dynamic and self-relevant. Here participants experienced several ambiguous tasks and subsequently viewed SenseCam footage of the same tasks, paired with negative or positive captions. Participants were trained to use mental imagery to inter-relate SenseCam footage and captions. Participants reported increased levels of happy mood, reduced levels of sad mood, and increased task enjoyment following SenseCam review with positive versus negative captions. This shift in emotional bias was also evident at 24-hour follow-up, as participants recollected greater task enjoyment for those tasks previously paired with positive captions. Mental imagery appears to play an important role in this process. These preliminary results indicate that in healthy volunteers, SenseCam can be used within a bias modification paradigm to shift mood and memory for wellbeing associated with performing everyday activities. Further refinements are necessary before similar methods can be applied to individuals suffering from subclinical and clinical depression.
PMCID: PMC3534350  PMID: 21416451
SenseCam; Cognitive bias modification; Emotion; Mental imagery
22.  Emotion Enhances the Subjective Feeling of Remembering, Despite Lower Accuracy for Contextual Details 
Emotion (Washington, D.C.)  2011;11(3):10.1037/a0024246.
Emotion strengthens the subjective experience of recollection. However, these vivid and confidently remembered emotional memories may not necessarily be more accurate. We investigated whether the subjective sense of recollection for negative stimuli is coupled with enhanced memory accuracy for contextual details using the remember/know paradigm. Our results indicate a double-dissociation between the subjective feeling of remembering, and the objective memory accuracy for details of negative and neutral scenes. “Remember” judgments were boosted for negative relative to neutral scenes. In contrast, memory for contextual details and associative binding was worse for negative compared to neutral scenes given a “remember” response. These findings show that the enhanced subjective recollective experience for negative stimuli does not reliably indicate greater objective recollection, at least of the details tested, and thus may be driven by a different mechanism than the subjective recollective experience for neutral stimuli.
PMCID: PMC3864593  PMID: 21668106
emotion; memory; subjective sense of remembering; remember/know; confidence
23.  Cold-Pressor Stress After Learning Enhances Familiarity-Based Recognition Memory in Men 
Neurobiology of learning and memory  2013;106:10.1016/j.nlm.2013.06.011.
Stress that is experienced after items have been encoded into memory can protect memories from the effects of forgetting. However, very little is known about how stress impacts recognition memory. The current study investigated how an aversive laboratory stressor (i.e., the cold-pressor test) that occurs after information has been encoded into memory affects subsequent recognition memory in an immediate and a delayed test (i.e., 2-hour and 3-month retention interval). Recognition was assessed for negative and neutral photographs using a hybrid remember/know confidence procedure in order to characterize overall performance and to separate recollection- and familiarity-based responses. The results indicated that relative to a non-stress control condition, post-encoding stress significantly improved familiarity but not recollection-based recognition memory or free recall. The beneficial effects of stress were observed in males for negative and neutral materials at both immediate and long-term delays, but were not significant in females. The results indicate that aversive stress can have long-lasting beneficial effects on the memory strength of information encountered prior to the stressful event.
PMCID: PMC3844034  PMID: 23823181
Recognition; Memory; Stress
24.  Attention during memory retrieval enhances future remembering 
Memory & cognition  2009;37(7):953-961.
Memory retrieval is a powerful learning event that influences whether an experience will be remembered in the future. Although retrieval can succeed in the presence of distraction, dividing attention during retrieval may reduce the power of remembering as an encoding event. In the present experiments, participants studied pictures of objects under full attention and then engaged in item recognition and source memory retrieval under full or divided attention. Two days later, a second recognition and source recollection test assessed the impact of attention during initial retrieval on long-term retention. On this latter test, performance was superior for items that had been tested initially under full versus divided attention. More importantly, even when items were correctly recognized on the first test, divided attention reduced the likelihood of subsequent recognition on the second test. The same held true for source recollection. Additionally, foils presented during the first test were also less likely to be later recognized if they had been encountered initially under divided attention. These findings demonstrate that attentive retrieval is critical for learning through remembering.
PMCID: PMC2776078  PMID: 19744935
25.  Right parietal cortex mediates recognition memory for melodies 
The European Journal of Neuroscience  2015;42(1):1660-1666.
Functional brain imaging studies have highlighted the significance of right‐lateralized temporal, frontal and parietal brain areas for memory for melodies. The present study investigated the involvement of bilateral posterior parietal cortices (PPCs) for the recognition memory of melodies using transcranial direct current stimulation (tDCS). Participants performed a recognition task before and after tDCS. The task included an encoding phase (12 melodies), a retention period, as well as a recognition phase (24 melodies). Experiment 1 revealed that anodal tDCS over the right PPC led to a deterioration of overall memory performance compared with sham. Experiment 2 confirmed the results of Experiment 1 and further showed that anodal tDCS over the left PPC did not show a modulatory effect on memory task performance, indicating a right lateralization for musical memory. Furthermore, both experiments revealed that the decline in memory for melodies can be traced back to an interference of anodal stimulation on the recollection process (remember judgements) rather than to familiarity judgements. Taken together, this study revealed a causal involvement of the right PPC for memory for melodies and demonstrated a key role for this brain region in the recollection process of the memory task.
PMCID: PMC4737257  PMID: 25959620
human; memory for melodies; posterior parietal cortex; recognition; recollection; transcranial direct current stimulation

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