Effects of modality on the neural correlates of encoding processes supporting recollection and familiarity

Prior research has demonstrated that the neural correlates of successful encoding ("subsequent memory effects") partially overlap with neural regions selectively engaged by the on-line demands of the study task. The primary goal of the present experiment was to determine whether this overlap is associated solely with encoding processes supporting later recollection, or whether overlapping subsequent memory and study condition effects are also evident when later memory is familiarity-based. Subjects (N = 17) underwent fMRI scanning while studying a series of visually and auditorily presented words. Memory for the words was subsequently tested with a modified Remember/Know procedure. Auditorily selective subsequent familiarity effects were evident in bilateral temporal regions that also responded preferentially to auditory items. Although other interpretations are possible, these findings suggest that overlap between study condition-selective subsequent memory effects and regions selectively sensitive to study demands is not uniquely associated with later recollection. In addition, modality-independent subsequent memory effects were identified in several cortical regions. In every case, the effects were greatest for later recollected items, and smaller for items later recognized on the basis of familiarity. The implications of this quantitative dissociation for dual-process models of recognition memory are discussed.     

FUNCTIONAL MAGNETIC RESONANCE IMAGING OF SEMANTIC MEMORY PROCESSES IN THE FRONTAL LOBES

Abstract— Frontal-lobe activation during semantic memory performance was examined using functional magnetic resonance imaging (fMRI), a noninvasive technique for localizing neural activity associated with cognitive function. Left inferior prefrontal cortex was more activated for semantic than for perceptual encoding of words, and for initial than for repeated semantic encoding of words. Decreased activation for semantic encoding of repeated words reflects repetition priming, that is, implicit retrieval of memory gained in the initial semantic encoding of a word. The left inferior prefrontal region may sub-serve semantic working memory processes that participate in semantic encoding and that have decreased demands when such encoding can be facilitated by recent semantic experience. These results demonstrate that fMRI can visualize changes in an individual's brain function associated with the encoding and retrieval of new memories.     

Lateral and medial prefrontal contributions to emotion generation by semantic elaboration during episodic encoding

Memories for emotion-laden stimuli are remembered more accurately than those for neutral stimuli. Although this enhancement reflects stimulus-driven modulation of memory by emotions, functional neuroimaging evidence of the interacting mechanisms between emotions generated by intentional processes, such as semantic elaboration, and memory is scarce. The present fMRI study investigated how encoding-related activation is modulated by emotions generated during the process of semantic elaboration. During encoding with fMRI, healthy young adults viewed neutral (target) pictures either passively or with semantic elaboration. In semantic elaboration, participants imagined background stories related to the pictures. Encoding trials with semantic elaboration were subdivided into conditions in which participants imagined negative, positive, or neutral stories. One week later, memories for target pictures were tested. In behavioral results, memories for target pictures were significantly enhanced by semantic elaboration, compared to passive viewing, and the memory enhancement was more remarkable when negative or positive stories were imagined. fMRI results demonstrated that activations in the left inferior frontal gyrus and dorsal medial prefrontal cortex (dmPFC) were greater during the encoding of target pictures with semantic elaboration than those with passive viewing, and that these activations further increased during encoding with semantic elaboration of emotional stories than of neutral stories. Functional connectivity between the left inferior frontal gyrus and dmPFC/hippocampus during encoding significantly predicted retrieval accuracies of memories encoded with self-generated emotional stories. These findings suggest that networks including the left inferior frontal region, dmPFC, and hippocampus could contribute to the modulation of memories encoded with the emotion generation.     

The role of attention in remembering important item-location associations

When encountering an excess of information, people are able to selectively remember high-value information by strategically allocating attention during the encoding period, termed value-directed remembering. This has been demonstrated in both the episodic verbal and visuospatial memory domains. Importantly, the allocation of attention also plays a crucial role in the binding of identity and location information in visuospatial memory. We examined how taxing attentional resources to various degrees during encoding might affect visuospatial memory and selectivity. Participants studied items paired with point values indicating their value in a grid display and were asked to maximize their point score (a summation of the points associated with correctly remembered information). Participants viewed items under either a sequential or simultaneous presentation format and in either the presence or absence of a secondary tone discrimination task. While participants in the divided attention conditions recalled fewer item-location associations overall, participants in all encoding conditions prioritized high-value information in memory, providing further evidence that selectivity can be maintained even when attentional resources are taxed. However, differences between presentation formats emerged when conducting spatial resolution analyses examining errors. Errors in the simultaneous conditions were only influenced by item value when attention was full during encoding, while errors in the sequential conditions were not influenced by item value, regardless of available attentional resources. The results suggest participants can strategically allocate attention during encoding even under cognitively-demanding conditions and that gist-based visuospatial memory may only be influenced by information importance when adequate attentional resources are available.     

Activation of midbrain structures by associative novelty and the formation of explicit memory in humans

Recent evidence suggests a close functional relationship between memory formation in the hippocampus and dopaminergic neuromodulation originating in the ventral tegmental area and medial substantia nigra of the midbrain. Here we report midbrain activation in two functional MRI studies of visual memory in healthy young adults. In the first study, participants distinguished between familiar and novel configurations of pairs of items which had been studied together by either learning the location or the identity of the items. In the second study, participants studied words by either rating the words' pleasantness or counting syllables. The ventral tegmental area and medial substantia nigra showed increased activation by associative novelty (first study) and subsequent free recall performance (second study). In both studies, this activation accompanied hippocampal activation, but was unaffected by the study task. Thus midbrain regions seem to participate selectively in hippocampus-dependent processes of associative novelty and explicit memory formation, but appear to be unaffected by other task-relevant aspects.     

How do students improve their value-based learning with task experience?

When learning items that vary in reward, students improve their scores (i.e., earned reward) with task experience. In four experiments, we examined whether such improvements arise from better selective encoding of items that would earn more (vs. less) reward. Participants studied and recalled words across multiple study-test trials. On each trial, 12 words were slated with different values (typically from 1 to 12), and participants earned the point value assigned to a given word if it was correctly recalled. In all experiments, participants earned more points across the first two trials. In Experiment 1, participants either self-paced their study or had experimenter-paced study and in Experiment 2, some participants were penalised for each second spent during study. Improvements in points earned were related to increases in overall recall but not to selective encoding. In Experiment 3, some participants were given value-emphasised instructions, yet they did not demonstrate selective encoding. In Experiment 4, we used a larger range of point values, but selective encoding still did not account for the improvement in point scores across lists. These results suggest that metacognitively-driven selective encoding is not necessary to observe improvements in value-based learning.     

Short theta burst stimulation to left frontal cortex prior to encoding enhances subsequent recognition memory

Deep semantic encoding of verbal stimuli can aid in later successful retrieval of those stimuli from long-term episodic memory. Evidence from numerous neuropsychological and neuroimaging experiments demonstrate regions in left prefrontal cortex, including left dorsolateral prefrontal cortex (DLPFC), are important for processes related to encoding. Here, we investigated the relationship between left DLPFC activity during encoding and successful subsequent memory with transcranial magnetic stimulation (TMS). In a pair of experiments using a 2-session within-subjects design, we stimulated either left DLPFC or a control region (Vertex) with a single 2-s train of short theta burst stimulation (sTBS) during a semantic encoding task and then gave participants a recognition memory test. We found that subsequent memory was enhanced on the day left DLPFC was stimulated, relative to the day Vertex was stimulated, and that DLPFC stimulation also increased participants’ confidence in their decisions during the recognition task. We also explored the time course of how long the effects of sTBS persisted. Our data suggest 2 s of sTBS to left DLPFC is capable of enhancing subsequent memory for items encoded up to 15 s following stimulation. Collectively, these data demonstrate sTBS is capable of enhancing long-term memory and provide evidence that TBS protocols are a potentially powerful tool for modulating cognitive function.     

Aging effects on memory encoding in the frontal lobes

Functional magnetic resonance imaging (fMRI) was used to compare frontal-lobe activation in younger and older adults during encoding of words into memory. Participants made semantic or nonsemantic judgments about words. Younger adults exhibited greater activation for semantic relative to nonsemantic judgments in several regions, with the largest activation in the left inferior frontal gyrus. Older adults exhibited greater activation for semantic judgments in the same regions. but the extent of activation was reduced in left prefrontal regions. In older adults, there was a significant association between behavioral tests of declarative and working memory and extent of frontal activation. These results suggest that age-associated decreases in memory ability may be due to decreased frontal-lobe contributions to the initial encoding of experience.     

The development of memory efficiency and value-directed remembering across the life span: a cross-sectional study of memory and selectivity

Although attentional control and memory change considerably across the life span, no research has examined how the ability to strategically remember important information (i.e., value-directed remembering) changes from childhood to old age. The present study examined this in different age groups across the life span (N = 320, 5-96 years old). A selectivity task was used in which participants were asked to study and recall items worth different point values in order to maximize their point score. This procedure allowed for measures of memory quantity/capacity (number of words recalled) and memory efficiency/selectivity (the recall of high-value items relative to low-value items). Age-related differences were found for memory capacity, as young adults recalled more words than the other groups. However, in terms of selectivity, younger and older adults were more selective than adolescents and children. The dissociation between these measures across the life span illustrates important age-related differences in terms of memory capacity and the ability to selectively remember high-value information.     

Exploring the role of attention during memory retrieval: Effects of semantic encoding and divided attention

Research on attention and memory suggests that semantic encoding leads to retrieval that is highly susceptible to divided attention. Three experiments tested this proposition and showed that dividing attention did not selectively affect semantically encoded items. Participants encoded a list of words in one of two ways: semantically or phonetically. Later, memory was assessed using either a standard recognition test (Experiment 1) or a rhyme recognition test (Experiments 2 and 3). The participants took the memory test either alone (full attention) or while simultaneously performing a secondary task (divided attention). Recognition accuracy was reduced by divided attention on both recognition tests, and semantically and phonetically encoded words were equally affected.     

Episodic encoding and recognition of pictures and words: role of the human medial temporal lobes

In the present PET study, we examined brain activity related to processing of pictures and printed words in episodic memory. Our goal was to determine how the perceptual format of objects (verbal versus pictorial) is reflected in the neural organization of episodic memory for common objects. We investigated this issue in relation to encoding and recognition with a particular focus on medial temporal-lobe (MTL) structures. At encoding, participants saw pictures of objects or their written names and were asked to make semantic judgments. At recognition, participants made yes-no recognition judgments in four different conditions. In two conditions, target items were pictures of objects; these objects had originally been encoded either in picture or in word format. In two other conditions, target items were words; they also denoted objects originally encoded either as pictures or as words. Our data show that right MTL structures are differentially involved in picture processing during encoding and recognition. A posterior MTL region showed higher activation in response to the presentation of pictures than of words across all conditions. During encoding, this region may be involved in setting up a representation of the perceptual information that comprises the picture. At recognition, it may play a role in guiding retrieval processes based on the perceptual input, i.e. the retrieval cue. Another more anterior right MTL region was found to be differentially involved in recognition of objects that had been encoded as pictures, irrespective of whether the retrieval cue provided was pictorial or verbal in nature; this region may be involved in accessing stored pictorial representations. Our results suggest that left MTL structures contribute to picture processing only during encoding. Some regions in the left MTL showed an involvement in semantic encoding that was picture specific; others showed a task-specific involvement across pictures and words. Together, our results provide evidence that the involvement of some but not all MTL regions in episodic encoding and recognition is format specific.     

“Wanted!” The effects of reward on face recognition: electrophysiological correlates

The aim of the present study was to uncover the temporal dynamics of face recognition as a function of reward. Event-related potentials (ERPs) were recorded during the encoding and the subsequent old/new memory test in response to faces that could be associated with a monetary reward. The behavioral results showed that faces associated with reward at both encoding and retrieval were recognized better than the unrewarded ones. ERP responses highlighted that successful encoding predictive of subsequent memory was greater for faces associated with reward than for faces without reward-driven motivational learning. At retrieval, an early positive-going component was elicited for potentially rewarded faces on frontal regions, while the occipito-temporal N170 component showed priming effects as a function of reward. Later on, larger centro-parietal ERP components, related to recognition memory, were found selectively for reward-associated faces. Remarkably, electrophysiological responses varied in a graded manner, with the largest amplitude yielded by faces with double reward, followed by faces associated with reward only at encoding. Taken together, the present data show that the processing of outcome expectations affects face structural encoding and increases memory efficiency, yielding a robust and sustained modulation over frontal and temporal areas where reward and memory mechanisms operate in conjunction.     

一致性、相关性对记忆生存优势效应的影响

对词语进行生存加工能提高记忆成绩,这种记忆的生存优势效应已得到不少研究的验证,且大多数研究表明生存优势是一种独特的编码方式(Nairne&Pandeirada,2011)。但是,Butler等人(2009)的研究结果表明实验中生存加工带来的记忆优势可能是一致性效应(即编码任务与编码的材料之间具有一致性)的作用。本文在2个实验中选用与生存和抢劫加工条件相关程度不同的词(高中低)为实验材料,采用生存加工、抢劫加工、愉悦度和有意学习为实验条件,研究一致性和相关性在记忆生存优势中的作用。结果发现:(1)生存条件下的记忆效果显著优于愉悦度条件和有意学习条件,这说明的确存在记忆的生存优势效应;(2)高生存相关词在生存加工条件下产生了记忆优势,而中、低生存相关词在2种加工条件下记忆成绩差异不显著,这说明加工条件的一致性只在一定程度上影响着记忆的生存优势效应;(3)词语自身的生存相关性没有表现出较强的记忆优势,当然这也可能与实验材料的词频有关。研究结果支持了Nairne和Pandeirada(2011)的观点。     

Is the enhancement of memory due to reward driven by value or salience?

Past research using two levels of reward has shown that the higher-value items are remembered better than lower-value items and this enhancement is assumed to be driven by an effect of reward value. In the present study, multiple levels of reward were used to test the influence of reward salience on memory. Using a value-learning procedure, words were associated with reward values, and then memory for these words was later tested with free recall. Critically, multiple reward levels were used, allowing us to test two specific hypotheses whereby rewards can influence memory: (a) higher value items are remembered better than lower value items (reward value hypothesis), and (b) highest and lowest value items are remembered best and intermediate-value items are remembered worst (following a U-shaped relationship between value and memory; reward salience hypothesis). In two experiments we observed a U-shaped relationship between reward value and memory, supporting the notion that memory is enhanced due to reward salience, and not purely through reward value.     

Hemispheric asymmetry in recognition memory: effects of retention level on the recognition of Portuguese words

Early findings from Broca and Wernicke led to the classical view of hemispheric specialization, where the main idea relates to left-hemisphere language capabilities compared to right-hemisphere visual capabilities. Federmeier and Benjamin (2005) have suggested that semantic encoding for verbal information in the right hemisphere can be more effective when memory demands are higher. In light of this, our main goal was to study the effect of retention level of verbal information on hemispheric processes. However, regarding the cross-linguistic differences in orthography and their subsequent effects on word recognition (Frost, Katz, & Bentin, 1987), our intent was also to test prior predictions of Federmeier and Benjamin (2005) for a "shallow" orthography language, where words have a clear correspondence between graphemes and phonemes, as opposed to English, which is a "deep" orthography language. Portuguese concrete nouns were selected. The participants were submitted to a visual half-field word presentation using a continuous recognition memory paradigm. The retention level included 1, 2, 4, 8, 20 or 40 words. Results showed that recognition accuracy was higher for words studied in the right visual field, compared to those studied in the left visual field, when the retention interval included 2, 4, or 20 words. No significant differences were found for the remaining intervals. Further analysis on accuracy data for intermediate retention levels showed that recognition accuracy was higher for the 2 words retention level than for the levels including 4, 8, or 20 words; it was higher for left-hemisphere encoding as well. Our results also indicated that reaction times were slower for left-hemisphere encoding and for the 40 words retention level when compared to that of 20 words. In summary, the current results are in partial agreement with those of Federmeier and Benjamin (2005) and suggest different hemispheric memory strategies for the semantic encoding of verbal information.     

注意促进效应的ERP研究

近期发现,采用目标探测任务作为二级任务时,目标探测条件不仅不会削弱,甚至会提高记忆成绩,产生注意促进效应（ABE）。为进一步探究目标探测的作用机制,研究采用事件相关电位（ERP）技术,对比目标与分心条件在编码和提取过程中所诱发的ERP差异。结果表明,两类条件在再认过程中所诱发的ERP差异不仅表现在早期与知觉加工相关的ERP成份上,并且一直持续到了后期与细节提取相关的ERP成分上。由此推测,ABE不仅体现在编码早期的知觉加工阶段,更会延续到后期的复述与精加工。     

Immediate memory consequences of the effect of emotion on attention to pictures

Emotionally arousing stimuli are at once both highly attention grabbing and memorable. We examined whether emotional enhancement of memory (EEM) reflects an indirect effect of emotion on memory, mediated by enhanced attention to emotional items during encoding. We tested a critical prediction of the mediation hypothesis-that regions conjointly activated by emotion and attention would correlate with subsequent EEM. Participants were scanned with fMRI while they watched emotional or neutral pictures under instructions to attend to them a lot or a little, and were then given an immediate recognition test. A region in the left fusiform gyrus was activated by emotion, voluntary attention, and subsequent EEM. A functional network, different for each attention condition, connected this region and the amygdala, which was associated with emotion and EEM, but not with voluntary attention. These findings support an indirect cortical mediation account of immediate EEM that may complement a direct modulation model.     

The question shapes the answer: the neural correlates of task differences reveal dynamic semantic processing

Task effects in semantic processing were investigated by contrasting the neural activation associated with two semantic categorization tasks (SCT) using event-related fMRI. The two SCTs involved different decision categories: is it an animal? vs. is it a concrete thing? Participants completed both tasks and, across participants, the same core set of items were presented in both tasks. Results showed task differences in the neural activation associated with these items: in the animal SCT there was greater activation in a number of frontal and temporal regions, including left superior and middle temporal gyri, while in the concrete SCT there was greater activation in left medial frontal gyrus and bilaterally in the precentral gyri. These results are interpreted as evidence of top-down modulation of semantic processing; participants make adjustments to optimize performance in a given task and these adjustments have consequences for the activation observed.     

The effects of aging on selectivity and control in short-term recall

The ability to control encoding and retrieval processing strategically is critical for the efficient use of memory. We examined the ability of younger and older adults to selectively remember words on the basis of their arbitrary point values by using a technique developed by Watkins and Bloom (1999). In the first three experiments, younger subjects recalled more words than did older subjects, but an independent index of recall selectivity showed that older subjects were apparently more successful in selecting higher valued words. However, a fourth experiment showed that this superior selectivity on the part of older adults was attributable to their greater proportional reliance on primary memory recall. Overall, the data suggest that although older adults recall fewer words than do younger adults, they exert as much control over some aspects of encoding.     

Monetary rewards influence retrieval orientations

Reward anticipation during learning is known to support memory formation, but its role in retrieval processes is so far unclear. Retrieval orientations, as a reflection of controlled retrieval processing, are one aspect of retrieval that might be modulated by reward. These processes can be measured using the event-related potentials (ERPs) elicited by retrieval cues from tasks with different retrieval requirements, such as via changes in the class of targeted memory information. To determine whether retrieval orientations of this kind are modulated by reward during learning, we investigated the effects of high and low reward expectancy on the ERP correlates of retrieval orientation in two separate experiments. The reward manipulation at study in Experiment 1 was associated with later memory performance, whereas in Experiment 2, reward was directly linked to accuracy in the study task. In both studies, the participants encoded mixed lists of pictures and words preceded by high- or low-reward cues. After 24?h, they performed a recognition memory exclusion task, with words as the test items. In addition to a previously reported material-specific effect of retrieval orientation, a frontally distributed, reward-associated retrieval orientation effect was found in both experiments. These findings suggest that reward motivation during learning leads to the adoption of a reward-associated retrieval orientation to support the retrieval of highly motivational information. Thus, ERP retrieval orientation effects not only reflect retrieval processes related to the sought-for materials, but also relate to the reward conditions with which items were combined during encoding.