The role of prefrontal cortex during tests of episodic memory

Recent studies of episodic memory using functional neuroimaging techniques indicate that right prefrontal cortex (PFC) is activated while people remember events. Our review suggests that left PFC is also activated during remembering, depending on the reflective demands of the task. As more, or more complex, reflective processes are required (e.g. when criteria for evaluation have to be established and maintained, when the complexity of the evaluation required increases, and when retrieval of additional information is required beyond that activated by an initial cue), left PFC activity is more likely to occur. Our `cortical asymmetry of reflective activity' (CARA) hypothesis summarizes available findings and suggests directions for future research.     

Functional asymmetry of human prefrontal cortex: encoding and retrieval of verbally and nonverbally coded information

There are several views about the organization of memory functions in the human prefrontal cortex. One view assumes a process-specific brain lateralization according to different memory subprocesses, that is, encoding and retrieval. An alternative view emphasizes content-specific lateralization of brain systems involved in memory processes. This study addresses this apparent inconsistency between process- and content-specific lateralization of brain activity by investigating the effects of verbal and nonverbal encoding on prefrontal activations during encoding and retrieval of environmental novel sounds using fMRI. An intentional memory task was applied in which subjects were required either to judge the sounds' loudness (nonverbal encoding task) or to indicate whether or not a sound can be verbally described (verbal encoding task). Retrieval processes were examined in a subsequent yes/no recognition test. In the study phase the right posterior dorsolateral prefrontal cortex (PFC) was activated in both tasks. During verbal encoding additional activation of the left dorsolateral PFC was obtained. Retrieval-related fMRI activity varied as a function of encoding task: For the nonverbal task we detected an activation focus in the right posterior dorsolateral PFC whereas an activation in the left dorsolateral PFC was observed for the verbal task. These findings indicate that the right dorsolateral PFC is engaged in encoding of auditory information irrespective of encoding task. The lateralization of PFC activity during retrieval was shown to depend on the availability of verbal codes, with left hemispheric involvement for verbally and right hemispheric activation for nonverbally coded information.     

工作记忆与情景记忆中脑区的重合与分离——从脑区定位看两者关系

尽管近期的研究结果认为前额叶在工作记忆和情景记忆任务中均被激活,但是仍然不清楚是否有特定的区域对两种记忆起着不同作用。对于工作记忆和情景记忆在脑区上的重合,研究者们做出了不同的解释。某些研究者认为脑区的重合反映了包含于情景记忆中的工作记忆的作用,另一些研究者则认为这种重合反映的是与工作记忆和情景记忆都有关的反省过程的性质。对此,作者提出了相应的讨论意见。     

Using fMRI to investigate

Using fMRI, we investigated the functional organization of prefrontal cortex (PFC) as participants briefly thought of a single just-experienced item (i.e., refreshed an active representation). The results of six studies, and a meta-analysis including previous studies, identified regions in left dorsolateral, anterior, and ventrolateral PFC associated in varying degrees with refreshing different types of information (visual and auditory words, drawings, patterns, people, places, or locations). In addition, activity increased in anterior cingulate with selection demands and in orbitofrontal cortex when a nonselected item was emotionally salient, consistent with a role for these areas in cognitive control (e.g., overcoming “mental rubbernecking”). We also found evidence that presenting emotional information disrupted an anterior component of the refresh circuit. We suggest that refreshing accounts for some neural activity observed in more complex tasks, such as working memory, long-term memory, and problem solving, and that its disruption (e.g., from aging or emotion) could have a broad impact.     

Human trace fear conditioning: right-lateralized cortical activity supports trace-interval processes

Pavlovian conditioning requires the convergence and simultaneous activation of neural circuitry that supports conditioned stimulus (CS) and unconditioned stimulus (US) processes. However, in trace conditioning, the CS and US are separated by a period of time called the trace interval, and thus do not overlap. Therefore, determining brain regions that support associative learning by maintaining a CS representation during the trace interval is an important issue for conditioning research. Prior functional magnetic resonance imaging (fMRI) research has identified brain regions that support trace-conditioning processes. However, relatively little is known about whether this activity is specific to the trace CS, the trace interval, or both periods of time. The present study was designed to disentangle the hemodynamic response produced by the trace CS from that associated with the trace interval, in order to identify learning-related activation during these distinct components of a trace-conditioning trial. Trace-conditioned activity was observed within dorsomedial prefrontal cortex (PFC), dorsolateral PFC, insula, inferior parietal lobule (IPL), and posterior cingulate (PCC). Each of these regions showed learning-related activity during the trace CS, while trace-interval activity was only observed within a subset of these areas (i.e., dorsomedial PFC, PCC, right dorsolateral PFC, right IPL, right superior/middle temporal gyrus, and bilateral insula). Trace-interval activity was greater in right than in left dorsolateral PFC, IPL, and superior/middle temporal gyrus. These findings indicate that components of the prefrontal, cingulate, insular, and parietal cortices support trace-interval processes, as well as suggesting that a right-lateralized fronto-parietal circuit may play a unique role in trace conditioning.     

Monitoring item and source information: Evidence for a negative generation effect in source memory

Item memory and source memory were assessed in a task that simulated a social conversation. Participants generated answers to questions or read statements presented by one of three sources (faces on a computer screen). Positive generation effects were observed for item memory. That is, participants remembered topics of conversation better if they were asked questions about the topics than if they simply read statements about topics. However, a negative generation effect occurred for source memory. That is, remembering the source of some information was disrupted if participants were required to answer questions pertaining to that information. These findings support the notion that item and source memory are mediated, as least in part, by different processes during encoding.     

Did I turn off the gas? Reality monitoring of everyday actions

Failing to remember whether we performed, or merely imagined performing, an everyday action can occasionally be inconvenient, but in some circumstances it can have potentially dangerous consequences. In this fMRI study, we investigated the brain activity patterns, and objective and subjective behavioral measures, associated with recollecting such everyday actions. We used an ecologically valid “reality-monitoring” paradigm in which participants performed, or imagined performing, specified actions with real objects drawn from one of two boxes. Lateral brain areas, including prefrontal cortex, were active when participants recollected both the actions that had been associated with objects and the locations from which they had been drawn, consistent with a general role in source recollection. By contrast, medial prefrontal and motor regions made more specific contributions, with supplementary motor cortex activity being associated with recollection decisions about actions but not locations, and medial prefrontal cortex exhibiting greater activity when remembering performed rather than imagined actions. These results support a theoretical interpretation of reality monitoring that entails the fine-grained discrimination between multiple forms of internally and externally generated information.     

Binding actions and scenes in visual long-term memory

How does visual long-term memory store representations of different entities (e.g., objects, actions, and scenes) that are present in the same visual event? Are the different entities stored as an integrated representation in memory, or are they stored separately? To address this question, we asked observers to view a large number of events; in each event, an action was performed within a scene. Afterward, the participants were shown pairs of action–scene sets and indicated which of the two they had seen. When the task required recognizing the individual actions and scenes, performance was high (80 %). Conversely, when the task required remembering which actions had occurred within which scenes, performance was significantly lower (59 %). We observed this dissociation between memory for individual entities and memory for entity bindings across multiple testing conditions and presentation durations. These experiments indicate that visual long-term memory stores information about actions and information about scenes separately from one another, even when an action and scene were observed together in the same visual event. These findings also highlight an important limitation of human memory: Situations that require remembering actions and scenes as integrated events (e.g., eyewitness testimony) may be particularly vulnerable to memory errors.     

Source monitoring and false memories in children: relation to certainty and executive functioning

We presented children aged 6, 8, and 10 years with a video and then an audio tape about a dog named Mick. Some information was repeated in the two sources and some was unique to one source. We examined: (a) children's hit rate for remembering whether events occurred and their tendency to make false alarms, (b) their memory for the context in which events occurred (source monitoring), (c) their certainty about hits, false alarms, and source, and (d) whether working memory and inhibition were related to hits, false alarms, and source monitoring. The certainty ratings revealed deficits in children's understanding of when they had erred on source questions and of when they had made false alarms. In addition, inhibitory ability accounted for unique variance in the ability to avoid false alarms and in some kinds of source monitoring but not hits. In contrast, working memory tended to correlate with all forms of memory including hits.     

Object-location memory: A lesion-behavior mapping study in stroke patients

Object-location memory is an important form of spatial memory, comprising different subcomponents that each process specific types of information within memory, i.e. remembering objects, remembering positions and binding these features in memory. In the current study we investigated the neural correlates of binding categorical (relative) or coordinate (exact) position information with objects in memory. Therefore, an object-location memory battery was used, including different task conditions assessing object-location memory, i.e. memory for position information per se, and binding object information with coordinate and categorical position information. Sixty-one stroke patients with focal brain lesions were examined and compared with 77 healthy matched controls. The lesion subtraction method was used to define the area of overlap. Results indicate an important role of the left posterior parietal cortex in the binding of both categorical and coordinate positions with object information. Additionally, the hippocampus seems important for categorical object-location memory. This suggests that categorical and coordinate object-location memory depend on similar cognitive and neural systems.     

Domain specificity in the primate prefrontal cortex

Experimental studies in nonhuman primates and functional imaging studies in humans have underlined the critical role played by the prefrontal cortex (PFC) in working memory. However, the precise organization of the frontal lobes with respect to the different types of information operated upon is a point of controversy, and several models of functional organizations have been proposed. One model, developed by Goldman-Rakic and colleagues, postulates a modular organization of working memory based on the type of information processing (the domain specificity hypothesis). Evidence to date has focused on the encoding of the locations of visual objects by the dorsolateral PFC, whereas the ventrolateral PFC is suggested to be involved in processing the features and identity of objects. In this model, domain should refer to any sensory modality that registers information relevant to that domain—for example, there would be visual and auditory input to a spatial information processing region and a feature analysis system. In support of this model, recent studies have described pathways from the posterior and anterior auditory association cortex that target dorsolateral spatial-processing regions and ventrolateral object-processing regions, respectively. In addition, physiological recordings from the ventrolateral PFC indicate that some cells in this region are responsive to the features of complex sounds. Finally, recordings in adjacent ventrolateral prefrontal regions have shown that the features of somatosensory stimuli can be discriminated and encoded by ventrolateral prefrontal neurons. These discoveries argue that two domains, differing with respect to the type of information being processed, and not with respect to the sensory modality of the information, are specifically localized to discrete regions of the PFC and embody the domain specificity hypothesis, first proposed by Patricia Goldman-Rakic.     

Electrophysiological correlates of encoding and retrieving emotional events

This study examined the impact of emotional content on encoding and retrieval processes. Event-related potentials were recorded in a source recognition memory task. During encoding, a posterior positivity for positive and negative pictures (250-450 ms) that presumably reflects attentional capturing of emotionally valenced stimuli was found. Additionally, positive events, which were also rated as less arousing than negative events, gave rise to anterior and posterior slow wave activity as compared with neutral and negative events and also showed enhanced recognition memory. It is assumed that positive low-arousing events enter controlled and elaborated encoding processes that are beneficial for recognition memory performance. The high arousal of negative events may interfere with controlled encoding mechanisms and attenuate item recognition and the quality of remembering. Moreover, topographically distinct late posterior negativities were obtained for the retrieval of the context features location and time that support the view that this component reflects processes in service of reconstructing the study episode by binding together contextual details with an item and that varies with the kind of episodic detail to be retrieved.     

Distinguishing the neural correlates of episodic memory encoding and semantic memory retrieval

Episodic memory and semantic memory interact very closely. In particular, episodic memory encoding (EE) tends to elicit semantic memory retrieval (SR), and vice versa. Thus, similar activations for EE and SR in functional neuroimaging studies may reflect shared memory processes, or they may reflect the fact that EE and SR are usually confounded. To address this issue, we used a factorial functional magnetic resonance imaging approach to disentangle the neural correlates of EE and SR. Within the left temporal lobe, the hippocampus was associated with successful EE, whereas a posterior lateral region was associated with successful SR. Within the left inferior prefrontal cortex, a posterior region was involved in SR, a mid region was involved in both SR and EE, and an anterior region was involved in EE, but only when SR was also high. Thus, the neural correlates of EE and SR are dissociable but interact in specific brain regions.     

Test modality affects source monitoring and event-related potentials

Two experiments investigated the effect of test modality (visual or auditory) on source memory and event-related potentials (ERPs). Test modality influenced source monitoring such that source memory was better when the source and test modalities were congruent. Test modality had less of an influence when alternative information (i.e., cognitive operations) could be used to inform source judgments in Experiment 2. Test modality also affected ERP activity. Variation in parietal ERPs suggested that this activity reflects activation of sensory information, which can be attenuated when the sensory information is misleading. Changes in frontal ERPs support the hypothesis that frontal systems are used to evaluate source-specifying information present in the memory trace.     

Hemifield asymmetries differentiate VSTM for single- and multiple-feature objects

Visual short-term memory (VSTM) is a capacity-limited system for maintaining visual information across brief durations. Limits in the amount of information held in memory reflect processing constraints in the intraparietal sulcus (IPS), a region of the frontoparietal network also involved in visual attention. During VSTM and visual attention, areas of IPS demonstrate hemispheric asymmetries. Whereas the left hemisphere represents information in only the right hemifield, the right hemisphere represents information across the visual field. In visual attention, hemispheric asymmetries are associated with differences in behavioral performance across the visual field. In order to assess the degree of hemifield asymmetries in VSTM, we measured memory performance across the visual field for both single- and two-feature objects. Consistent with theories of right-hemisphere dominance, there was a memory benefit for single-feature items in the left visual hemifield. However, when the number of features increased, the behavioral bias reversed, demonstrating a benefit for remembering two-feature objects in the right hemifield. On an individual basis, the cost of remembering an additional feature in the hemifields was correlated, suggesting that the shift in hemifield biases reflected a redistribution of resources across the visual field. Furthermore, we demonstrate that these results cannot be explained by differences in perceptual or decision-making load. Our results are consistent with a flexible resource model of VSTM in which attention and/or working memory demands result in representation of items in the right hemifield by both the left and right hemispheres.     

Parietal lobe contributions to episodic memory retrieval

Although the parietal lobe is not traditionally thought to support declarative memory, recent event-related fMRI studies of episodic retrieval have consistently revealed a range of memory-related influences on activation in lateral posterior parietal cortex (PPC) and precuneus extending into posterior cingulate and retrosplenial cortex. This article surveys the fMRI literature on PPC activation during remembering, a literature that complements earlier electroencephalography data. We consider these recent memory-related fMRI responses within the context of classical ideas about parietal function that emphasize space-based attention and motor intention. We conclude by proposing three hypotheses concerning how parietal cortex might contribute to memory.     

Maintenance versus manipulation of information held in working memory: an event-related fMRI study.

One model of the functional organization of lateral prefrontal cortex (PFC) in primates posits that this region is organized in a dorsal/ventral fashion subserving spatial and object working memory, respectively. Alternatively, it has been proposed that a dorsal/ventral subdivision of lateral PFC instead reflects the type of processing performed upon information held in working memory. We tested this hypothesis using an event-related fMRI method that can discriminate among functional changes occurring during temporally separated behavioral subcomponents of a single trial. Subjects performed a delayed-response task with two types of trials in which they were required to: (1) retain a sequence of letters across the delay period (maintenance) or (2) reorder the sequence into alphabetical order across the delay period (manipulation). In each subject, activity during the delay period was found in both dorsolateral and ventrolateral PFC in both types of trials. However, dorsolateral PFC activity was greater in manipulation trials. These findings are consistent with the processing model of the functional organization of working memory in PFC.     

Modulation of retrieval processing reflects accuracy of emotional source memory

There is considerable evidence that encoding and consolidation of memory are modulated by emotion, but the retrieval of emotional memories is not well characterized. Here we manipulated the emotional context with which affectively neutral stimuli were associated during encoding, allowing us to examine neural activity associated with retrieval of emotional memories without confounding the emotional attributes of cue items and the retrieved context. Using a source memory procedure we were also able to compare how retrieval processing was modulated when the emotional encoding context was recollected or not. An interaction between emotional encoding context and accuracy of source memory revealed that successful retrieval of emotional context was associated with activity in left amygdala, and a left frontotemporal network including anterior insula, prefrontal cortex and cingulate. In contrast, when contextual retrieval was unsuccessful, items encoded in emotional contexts elicited enhanced activity in right amygdala and a right-lateralized network that included extrastriate visual areas. These findings indicate distinct effects of emotion on successful and unsuccessful retrieval of source information, including lateralization of amygdala responses.     

Some surprising findings on the involvement of the parietal lobe in human memory

The posterior parietal lobe is known to play some role in a far-flung list of mental processes: linking vision to action (saccadic eye movements, reaching, grasping), attending to visual space, numerical calculation, and mental rotation. Here, we review findings from humans and monkeys that illuminate an untraditional function of this region: memory. Our review draws on neuroimaging findings that have repeatedly identified parietal lobe activations associated with short-term or working memory and episodic memory. We also discuss recent neuropsychological findings showing that individuals with parietal lobe damage exhibit both working memory and long-term memory deficits. These deficits are not ubiquitous; they are only evident under certain retrieval demands. Our review elaborates on these findings and evaluates various theories about the mechanistic role of the posterior parietal lobe in memory. The available data point towards the conclusion that the posterior parietal lobe plays an important role in memory retrieval irrespective of elapsed time. However, the available data do not support simple dichotomies such as recall versus recognition, working versus long-term memory. We conclude by formalizing several open questions that are intended to encourage future research in this rapidly developing area of memory research.     

Large,colorful, or noisy? Attribute- and modality-specific activations during retrieval of perceptual attribute knowledge

Position emission tomography was used to investigate whether retrieval of perceptual knowledge from long-term memory activates unique cortical regions associated with the modality and/or attribute type retrieved. Knowledge about the typical color, size, and sound of common objects and animals was probed, in response to written words naming the objects. Relative to a nonsemantic control task, all the attribute judgments activated similar left temporal and frontal regions. Visual (color, size) knowledge selectively activated the right posterior inferior temporal (PIT) cortex, whereas sound judgments elicited selective activation in the left posterior superior temporal gyrus and the adjacent parietal cortex. All of the attribute judgments activated a left PIT region, but color retrieval generated more activation in this area. Size judgments activated the right medial parietal cortex. These results indicate that the retrieval of perceptual semantic information activates not only a general semantic network, but also cortical areas specialized for the modality and attribute type of the knowledge retrieved.