Reactivation of schema representation in lateral occipital cortex supports successful memory encoding.

Schemas provide a scaffold onto which we can integrate new memories. Previous research has investigated the brain activity and connectivity underlying schema-related memory formation. However, how schemas are represented and reactivated in the brain, in order to enhance memory, remains unclear. To address this issue, we used an object-location spatial schema that was learned over multiple sessions, combined with similarity analyses of neural representations, to investigate the reactivation of schema representations of object-location memories when a new object-scene association is learned. In addition, we investigated how this reactivation affects subsequent memory performance under different strengths of schemas. We found that reactivation of a schema representation in the lateral occipital cortex (LOC) during object-scene encoding affected subsequent associative memory performance only in the schema-consistent condition and increased the functional connectivity between the LOC and the parahippocampal place area. Taken together, our findings provide new insight into how schema acts as a scaffold to support the integration of novel information into existing cortical networks and suggest a neural basis for schema-induced rapid cortical learning.

The influence of repeated study and repeated testing on the testing effect and the transfer effect over time.

Many studies have shown that compared to the restudy condition (RS), retrieval practice (RP) enhances the long-retention memory of retrieved items (i.e., the testing effect), and facilitates later memory of non-retrieved but related items (i.e., the transfer effect). However, previous studies have usually used repeated study and repeated testing, which are included in study-testing cycles. Therefore, it is unclear to what extent the factors of repeated study and repeated testing influence testing and transfer effects over time. In this study, participants studied sentences that described various episodes, then tested a half subset of the original sentences under three conditions (RP, RS, control). After retention intervals of 10 min, 1 day and 7 days, they recalled all of the information in the sentences. The results showed that the testing effect was enhanced by repeated study or repeated testing, while the transfer effect occurred only after both repeated study and repeated testing. Furthermore, repeated study or repeated testing slowed down the forgetting of retrieved items, while the forgetting of non-retrieved items occurred after both repeated study and repeated testing. The testing effect increased over time, but the transfer effect remained relatively stable over time. These results clarified different roles of multiple study repetitions and testing opportunities in the testing effect and the transfer effect, and suggest that the repeated retrieval could be combined with repeated study to optimally promote long-term retention of the memory of tested and non-tested items.

Learning from errors: Distinct neural networks for monitoring errors and maintaining corrects through repeated practice and feedback.

How memory representations are eventually established and maintained in the brain is one of central issues in memory research. Although the hippocampus and various brain regions have been shown to be involved in learning and memory, how they coordinate to support successful memory through errors is unclear. In this study, a retrieval practice (RP) - feedback (FB) paradigm was adopted to address this issue. Fifty-six participants (27 in the behavioral group, and 29 in the fMRI group) learned 120 Swahili-Chinese words associations and underwent two RP-answer FB cycles (i.e., RP1, FB1, RP2, FB2). The responses of the fMRI group were recorded in the fMRI scanner. The trials were divided based on participant's performance (correct or incorrect, C or I) during the two RPs and the final test (i.e., trial type, CCC, ICC, IIC III). The results showed that the regions in the salience and executive control networks (S-ECN) during RP, but not during FB, was strongly predictive of final successful memory. Their activation was just before the errors were corrected (i.e., RP1 in ICC trials and RP2 in IIC trials). The anterior insula (AI) is a core region in monitoring repeated errors, and it had differential connectivity with the default mode network (DMN) regions and the hippocampus during the RP and FB phases to inhibit incorrect answers and update memory. In contrast, maintaining corrected memory representation requires repeated RP and FB, which was associated with the DMN activation. Our study clarified how different brain regions support error monitoring and memory maintenance through repeated RP and FB, and emphasized the role of the insula in learning from errors.

Rapid acquisition through fast mapping: stable memory over time and role of prior knowledge.

In recent years, there have been intensive debates on whether healthy adults acquire new word knowledge through fast mapping (FM) by a different mechanism from explicit encoding (EE). In this study, we focused on this issue and investigated to what extent retention interval, prior knowledge (PK), and lure type modulated memory after FM and EE. Healthy young participants were asked to learn novel word-picture associations through both FM and EE. Half of the pictures were from familiar categories (i.e., high PK) and the other half were from unfamiliar categories (i.e., low PK). After 10 min and 1 wk, the participants were tested by forced-choice (FC) tasks, with lures from different categories (Experiment 1) or from the same categories of the target pictures (Experiment 2). Pseudowords were used to denote names of the novel pictures and baseline performance was controlled for each task. The results showed that in both Experiments 1 and 2, memory performance remained stable after FM, while it declined after EE from 10 min to 1 wk. Moreover, the effect of PK appeared at 10 min after FM while at 1 wk after EE in Experiment 2. PK enhanced memory of word-picture associations when the lures were from the same categories (Experiment 2), rather than from different categories (Experiment 1). These results were largely confirmed in Experiment 3 when encoding condition was manipulated as a between-subjects factor, while lure type as a within-subjects factor. The findings suggest that different from EE, FM facilitates rapid acquisition and consolidation of word-picture knowledge, and highlight that PK plays an important role in this process by enhancing access to detailed information.

Dissociation of the Perirhinal Cortex and Hippocampus During Discriminative Learning of Similar Objects.

Discriminative learning is a paradigm that has been used in animal studies, in which memory of a stimulus is enhanced when it is presented with a similar stimulus rather than with a different one. Human studies have shown that through discriminative learning of similar objects, both item memory and contextual memories are enhanced. However, the underlying neural mechanisms for it are unclear. The hippocampus and perirhinal cortex (PRC) are two possible regions involved in discriminating similar stimuli and forming distinctive memory representations. In this study, 28 participants (15 males) were scanned using high-resolution fMRI when a picture (e.g., a dog) was paired with the same picture, with a similar picture of the same concept (e.g., another dog), or with a picture of a different concept (e.g., a cat). Then, after intervals of 20 min and 1 week, the participants were asked to perform an old/new recognition task, followed by a contextual judgment. The results showed that during encoding, there was stronger activation in the PRC for the "similar" than for the "same" and "different" conditions and it predicted subsequent item memory for the "similar" condition. The hippocampal activation decreased for the "same" versus the "different" condition and the DG/CA3 activation predicted subsequent contextual memory for the "similar" condition. These results suggested that the PRC and hippocampus are functionally dissociated in encoding simultaneously presented objects and predicting subsequent item and contextual memories after discriminative learning.SIGNIFICANCE STATEMENT How the brain separates similar input into nonoverlapping representations and forms distinct memory for them is a fundamental question for the neuroscience of memory. By discriminative learning of similar (vs different) objects, both item and contextual memories are enhanced. This study found functional dissociations between perirhinal cortex (PRC) and hippocampus in discriminating pairs of similar and different objects and in predicting subsequent memory of similar objects in their item and contextual aspects. The results provided clear evidence on the neural mechanisms of discriminative learning and highlighted the importance of the PRC and hippocampus in processing different types of object information when the objects were simultaneously presented.

Role of the hippocampus in the spacing effect during memory retrieval.

It is well known that distributed learning (DL) leads to improved memory performance compared with massed learning (ML) (i.e., spacing effect). However, the extent to which the hippocampus is involved in the spacing effect at shorter and longer retention intervals remains unclear. To address this issue, two groups of participants were asked to encode face-scene pairs at 20-min, 1-day, and 1-month intervals before they were scanned using fMRI during an associative recognition task. The pairs were repeated six times in either a massed (i.e., six times in 1 day) or a distributed (i.e., six times over 3 days, twice per day) manner. The results showed that compared with that in the ML group, the activation of the left hippocampus was stronger in the DL group when the participants retrieved old pairs correctly and rejected new pairs correctly at different retention intervals. In addition, the posterior hippocampus was more strongly activated when the new associations were rejected correctly after DL than ML, especially at the 1-month interval. Hence, our results provide evidence that the hippocampus is involved in better memory performance after DL compared to ML at both shorter and longer retention intervals.

Interplay of the long axis of the hippocampus and ventromedial prefrontal cortex in schema-related memory retrieval.

When new information is relevant to prior knowledge or schema, it can be learned and remembered better. Rodent studies have suggested that the hippocampus and ventromedial prefrontal cortex (vmPFC) are important for processing schema-related information. However, there are inconsistent findings from human studies on the involvement of the hippocampus and its interaction with the vmPFC in schema-related memory retrieval. To address these issues, we used a human analog of the rodent spatial schema task to compare brain activity during immediate retrieval of paired associations (PAs) in schema-consistent and schema-inconsistent conditions. The results showed that the anterior hippocampus was more involved in retrieving PAs in the schema-consistent condition than in the schema-inconsistent condition. Connectivity analyses showed that the anterior hippocampus had stronger coupling with the vmPFC when the participants retrieved newly learned PAs successfully in the schema-consistent (vs. schema-inconsistent) condition, whereas the coupling of the posterior hippocampus with the vmPFC showed the opposite. Taken together, the results shed light on how the long axis of the hippocampus and vmPFC interact to serve memory retrieval via different networks that differ by schema condition.

Discriminative learning of similar objects enhances memory for the objects and contexts.

How to improve our episodic memory is an important issue in the field of memory. In the present study, we used a discriminative learning paradigm that was similar to a paradigm used in animal studies. In Experiment 1, a picture (e.g., a dog) was either paired with an identical picture, with a similar picture of the same concept (e.g., another dog), or with a picture of a different concept (e.g., a cat). Then, after intervals of 10 min, 1 d, and 1 wk, participants were asked to perform a 2-alternative forced-choice (2AFC) task to discriminate between a repeated and a similar picture, followed by the contextual judgment. In Experiment 2, eye movements were measured when participants encoded the pairs of pictures. The results showed that by discriminative learning, there was better memory performance in the 2AFC task for the "same" and "similar" conditions than for the "different" condition. In addition, there was better contextual memory performance for the "similar" condition than for the other two conditions. With regard to the eye movements, the participants were more likely to fixate on the lure objects and made more saccades between the target and lure objects in the "similar" (versus "different") condition. The number of saccades predicted how well the targets were remembered in both the 2AFC and contextual memory tasks. These results suggested that with discriminative learning of similar objects, detailed information could be better encoded by distinguishing the object from similar interferences, making the details and the contexts better remembered and retained over time.

Context and Time Matter: Effects of Emotion and Motivation on Episodic Memory Overtime.

Previous studies have shown that compared with neutral cues, stimuli with positive and negative/stressful contexts or reward and punishment cues are remembered better. However, it is unclear whether the enhanced effect differs in emotion or motivation dimensions and the passage of time. We addressed these issues by manipulating different contextual cues for neutral words at different time intervals. In experiment 1, subjects were asked to learn words with picture contexts in positive, negative/stressful, and neutral valences and were tested by old/new word recognition and contextual judgment 10 min, 1 day, and 1 week later. In experiment 2, the reward and punishment motivations were manipulated by monetary cues during learning. Word recognition and contextual judgment were assessed 10 min, 1 day, 1 week, and 1 month after the study. Compared with negative and punishment conditions, the words in positive and reward contexts were recognized better at shorter intervals, which was associated with recollection process. In contrast, the words in negative and punishment contexts were recognized better at longer intervals, which was mainly associated with familiarity process. These results clarified how different dimensions of emotional and motivational contexts influence memory at short and long intervals and highlighted the role of contextual features in memory formation and consolidation.

Effects of Arousal and Context on Recognition Memory for Emotional Pictures in Younger and Older Adults.

Background/Study Context: Previous studies found that older adults tend to remember more positive than negative information (i.e., positivity bias), leading to an age-related positivity effect. However, the extent to which factors of arousal and contextual information influence the positivity bias in older adults remains to be determined. METHODS: In this study, 27 Chinese younger adults (20.00 ± 1.75 years) and 33 Chinese older adults (70.76 ± 5.49) learned pictures with negative, positive, and neutral valences. Half of the pictures had a human context, and the other half did not. In addition, emotional dimensions of negative and positive pictures were divided into high-arousal and low-arousal. The experimental task was to provide old/new recognition and confidence rating judgments. RESULTS: Both groups of subjects showed the positivity bias for low-arousal pictures, but the positivity bias was restricted to low-arousal pictures without the human context in older adults. In addition, the positivity bias was mainly driven by the recollection process in younger adults, and it was mainly driven by both the recollection and familiarity processes in older adults. The recognition of the nonhuman positive pictures was correlated with cognitive control abilities, but the recognition of pictures with human contexts was correlated with general memory abilities in older adults. CONCLUSION: This study highlights the importance of arousal and contextual information in modulating emotional memory in younger and older adults. It suggests that there are different mechanisms for memorizing pictures with and without human contexts in older adults.

Effects of learning experience on forgetting rates of item and associative memories.

Are associative memories forgotten more quickly than item memories, and does the level of original learning differentially influence forgetting rates? In this study, we addressed these questions by having participants learn single words and word pairs once (Experiment 1), three times (Experiment 2), and six times (Experiment 3) in a massed learning (ML) or a distributed learning (DL) mode. Then they were tested for item and associative recognition separately after four retention intervals: 10 min, 1 d, 1 wk, and 1 mo. The contribution of recollection and familiarity processes were assessed by participants' remember/know judgments. The results showed that for both item and associative memories, across different degrees of learning, recollection decreased significantly and was the main source of forgetting over time, whereas familiarity remained relatively stable over time. Learning multiple times led to slower forgetting at shorter intervals, depending on recollection and familiarity processes. Compared with massed learning, distributed learning (six times) especially benefited associative memory by increasing recollection, leading to slower forgetting at longer intervals. This study highlighted the importance of process contribution and learning experiences in modulating the forgetting rates of item and associative memories. We interpret these results within the framework of a dual factor representational model of forgetting (as noted in a previous study) in which recollection is more prone to decay over time than familiarity.

Recollection reduces unitised familiarity effect.

Two types of encoding tasks have been employed in previous research to investigate the beneficial effect of unitisation on familiarity-based associative recognition (unitised familiarity effect), namely the compound task and the interactive imagery task. Here we show how these two tasks could differentially engage subsequent recollection-based associative recognition and consequently lead to the turn-on or turn-off of the unitised familiarity effect. In the compound task, participants studied unrelated word pairs as newly learned compounds. In the interactive imagery task, participants studied the same word pairs as interactive images. An associative recognition task was used in combination with the Remember/Know procedure to measure recollection-based and familiarity-based associative recognition. The results showed that the unitised familiarity effect was present in the compound task but was absent in the interactive imagery task. A comparison of the compound and the interactive imagery task revealed a dramatic increase in recollection-based associative recognition for the interactive imagery task. These results suggest that unitisation could benefit familiarity-based associative recognition; however, this effect will be eliminated when the memory trace formed is easily accessed by strong recollection without the need for a familiarity assessment.

Distinct brain activity in processing negative pictures of animals and objects - the role of human contexts.

Previous studies have shown that the amygdala is important in processing not only animate entities but also social information. It remains to be determined to what extent the factors of category and social context interact to modulate the activities of the amygdala and cortical regions. In this study, pictures depicting animals and inanimate objects in negative and neutral levels were presented. The contexts of the pictures differed in whether they included human/human parts. The factors of valence, arousal, familiarity and complexity of pictures were controlled across categories. The results showed that the amygdala activity was modulated by category and contextual information. Under the nonhuman context condition, the amygdala responded more to animals than objects for both negative and neutral pictures. In contrast, under the human context condition, the amygdala showed stronger activity for negative objects than animals. In addition to cortical regions related to object action, functional and effective connectivity analyses showed that the anterior prefrontal cortex interacted more with the amygdala for negative objects (vs. animals) in the human context condition, by a top-down modulation of the anterior prefrontal cortex to the amygdala. These results highlighted the effects of category and human contexts on modulating brain activity in emotional processing.

Effects of memory cue and interest in remembering and forgetting of gist and details.

The gist and details of an event are both important for us to establish and maintain episodic memory. On the other hand, episodic memory is influenced by both external and internal factors, such as memory cue and intrinsic motivation. To what extent these factors and their interaction modulate memory and forgetting of gist and detailed information remains unclear. In this study, 29 participants watched film clips accompanied by either gist or detailed cues and rated their interest in these clips. Their memories of gist and detailed information were tested after 10 min, 1 day, and 1 week. The results showed that memory cue modulated the forgetting of gist and detailed memories. Specifically, when gist cues were used, gist memory was forgotten more slowly than detailed memory. When detailed cues were used, detailed memory was forgotten more slowly than gist memory. Differently, the subjective interest in the clips enhanced memory accuracy irrespective of memory type but did not influence the forgetting of gist and detailed memories. Moreover, there was a significant interaction between memory cue and interest, showing that gist cues enhanced memory than detailed cues only for low-interest clips. These results suggest that external and internal factors have differential effects on memory and forgetting, and the effectiveness of external factors depends on the state of intrinsic motivation. The significant interplay of different factors in influencing the remembering or forgetting of gist and detailed memories provides potential ways to enhance memory and retention of gist and detailed information.

Effects of schema on the relationship between post-encoding brain connectivity and subsequent durable memory.

Schemas can facilitate memory consolidation. Studies have suggested that interactions between the hippocampus and the ventromedial prefrontal cortex (vmPFC) are important for schema-related memory consolidation. However, in humans, how schema accelerates the consolidation of new information and relates to durable memory remains unclear. To address these knowledge gaps, we used a human analogue of the rodent spatial schema task and resting-state fMRI to investigate how post-encoding brain networks can predict long-term memory performance in different schema conditions. After participants were trained to obtain schema-consistent or schema-inconsistent object-location associations, they learned new object-location associations. The new associations were tested after the post-encoding rest in the scanner and 24 h later outside the scanner. The Bayesian multilevel modelling was applied to analyse the post-encoding brain networks. The results showed that during the post-encoding, stronger vmPFC- anterior hippocampal connectivity was associated with durable memory in the schema-consistent condition, whereas stronger object-selective lateral occipital cortex (LOC)-ventromedial prefrontal connectivity and weaker connectivity inside the default mode network were associated with durable memory in the schema inconsistent condition. In addition, stronger LOC-anterior hippocampal connectivity was associated with memory in both schema conditions. These results shed light on how schemas reconfigure early brain networks, especially the prefrontal-hippocampal and stimuli-relevant cortical networks and influence long-term memory performance.

Effects of prior knowledge on brain activation and functional connectivity during memory retrieval.

Previous studies have shown that the ventral medial prefrontal cortex (vmPFC) plays an important role in schema-related memory. However, there is an intensive debate to what extent the activation of subregions of the hippocampus is involved in retrieving schema-related memory. In addition, it is unclear how the functional connectivity (FC) between the vmPFC and the hippocampus, as well as the connectivity of the vmPFC with other regions, are modulated by prior knowledge (PK) during memory retrieval over time. To address these issues, participants learned paragraphs that described features of each unfamiliar word from familiar and unfamiliar categories (i.e., high and low PK conditions) 20 min, 1 day, and 1 week before the test. They then performed a recognition task to judge whether the sentences were old in the scanner. The results showed that the activation of the anterior-medial hippocampus (amHPC) cluster was stronger when the old sentences with high (vs. low) PK were correctly retrieved. The activation of the posterior hippocampus (pHPC) cluster, as well as the vmPFC, was stronger when the new sentences with high (vs. low) PK were correctly rejected (i.e., CR trials), whereas the cluster of anterior-lateral hippocampus (alHPC) showed the opposite. The FC of the vmPFC with the amHPC and perirhinal cortex/inferior temporal gyrus was stronger in the high (vs. low) PK condition, whereas the FC of the vmPFC with the alHPC, thalamus and frontal regions showed the opposite for the CR trials. This study highlighted that different brain networks, which were associated with the vmPFC, subregions of the hippocampus and cognitive control regions, were responsible for retrieving the information with high and low PK.

Beyond the hippocampus: boundary conditions for cortical connectivity and activity over time.

By including four different time intervals and controlling for behavioral confounds, Tallman et al. (this issue) found that brain connectivity of cortical regions with the vmPFC or with the hippocampus changed over time, although hippocampal activity did not change significantly. This study shed light on how memory is consolidated as it ages. Further studies could clarify the extent to which other factors, such as memory content, influence brain connectivity with more than two time intervals. The roles of different cortical regions in memory consolidation should also be addressed.

Effects of level of processing on emotional memory: gist and details.

The object of this study was to investigate whether level of processing (LOP) modulates enhanced memory performance for emotional stimuli, and, if so, whether the LOP effects relate to their gist and details. During the study phase, participants were presented with colourful pictures with negative, neutral and positive valences and encoded the emotional pictures under either a semantic (living/non-living judgement) or a perceptual (left/right position judgement) condition. During the test phase, they judged whether the presented picture was old or new in Experiments 1 and 2, and also judged whether a specific concept, labelled using words, had been studied in Experiment 2. The results showed that under both encoding conditions, the details of both negative and positive pictures were recognised better than those of neutral pictures. Also, the gist of negative pictures was recognised better than that of neutral pictures but only under the semantic condition. These data provide evidence that the LOP differentially modulates enhanced emotional memory for gist and details of pictures.

Effect of feedback type on enhancing subsequent memory: Interaction with initial correctness and confidence level.

Feedback is an important factor to enhance subsequent memory, showing that memory performance increases after the feedback than after the no feedback condition during retrieval practice. However, most studies have provided answers as feedback and only examined memory accuracy. It is unclear whether memory is enhanced over time when other types of feedback (e.g., correct/incorrect) is given. In addition, during retrieval practice, participants' responses differ in correctness and confidence level. To what extent these initial memory features interact with feedback type to influence subsequent memory accuracy and confidence level remains unclear. In this study, to address these questions, participants learned a series of sentences, then during the retrieval practice phase, different types of feedback-feedback with correct/incorrect and answer (CA-feedback), feedback with answer (A-feedback), feedback with correct/incorrect (C-feedback), and no feedback-were given after they performed a cued-recall test and rated the confidence. After retention intervals of 5 min, 1 day, and 7 days, they took final tests, followed by the confidence rating. The results showed that different types of feedback influenced subsequent memory and forgetting by different mechanisms. The CA-feedback and A-feedback enhanced memory performance by correcting initial errors and increasing the confidence of correct trials, but the corrected memory was more easily forgotten from 5 min to 7 days. Compared to A-feedback, the CA-feedback maintained the corrected memory after 1 day. The C-feedback did not correct initial errors but slowed the forgetting rate and reduced the confidence of incorrect trials. This study highlighted the interaction between feedback type and initial memory features (correctness, confidence) to influence subsequent memory performance, including memory accuracy and confidence level.

The effect of encoding task on the forgetting of object gist and details.

One important feature of episodic memory is that it contains fine-grained and vividly recollected details. How to improve and maintain detailed information over time has been one of the central issues in memory research. Previous studies have inconsistent findings on whether detailed memory is forgotten more rapidly than gist memory. In this study, we investigated to what extent different encoding tasks modulated forgetting of gist and detailed information. In three experiments, participants were presented pictures of common objects and were asked to name them (Experiment 1), describe the details about them (Experiment 2) or imagine scenes associated with them (Experiment 3). After intervals of 10 minutes, one day, one week and one month, gist and detailed memories of the pictures were tested and assessed using a remember/know/guess judgement. The results showed that after the naming task, gist and detailed memories were forgotten at a similar rate, but after the description and the imagination tasks, detailed memory was forgotten at a slower rate than gist memory. The forgetting rate of gist memory was the slowest after the naming task, while that of detailed memory was the slowest after the description task. In addition, when three experiments were compared, the naming task enhanced the contributions of recollection and familiarity for gist memory, while the description task enhanced the contribution of familiarity for detailed memory. These results reveal the importance of the encoding task in the forgetting of gist and detailed information, and suggest a possible way to maintain perceptual details of objects at longer intervals.