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Charan Ranganath
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Journal Articles
Tim Rüterbories, Axel Mecklinger, Kathrin C. J. Eschmann, Jordan Crivelli-Decker, Charan Ranganath ...
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Journal of Cognitive Neuroscience (2024) 36 (5): 888–900.
Published: 01 May 2024
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Successful learning depends on various factors such as depth of processing, motivation, or curiosity about information. A strong drive to learn something or the expectation of receiving a reward can be crucial to enhance learning. However, the influence of curiosity on the processing of new information and its similarity with reward processing is not well understood. This study examined whether states of curiosity influence specific ERPs associated with reward processing and whether these ERPs are related with later memory benefits. In an initial screening phase, participants indicated their curiosity and confidence in prior knowledge about answers to various trivia questions. In a subsequent study phase, we targeted different time windows related to reward processing during the presentation of trivia answers containing the reward positivity (RewP; 250–350 msec), the P3 (250–500 msec), and the late-positive-potential (LPP; 600–1000 msec). In a following surprise memory test, we found that participants recalled more high- than low-curiosity answers. The RewP, P3, and LPP showed greater positive mean amplitudes for high compared with low curiosity, reflecting increased reward processing. In addition, we found that the RewP and the P3 showed more positive mean amplitudes for later recalled compared with later forgotten answers, but curiosity did not modulate this encoding-related results. These findings support the view that the satisfaction of curiosity resembles reward processing, indicated by ERPs.
Journal Articles
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Journal of Cognitive Neuroscience (2022) 35 (1): 90–110.
Published: 01 December 2022
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The hippocampus plays a critical role in supporting episodic memory, in large part by binding together experiences and items with surrounding contextual information. At present, however, little is known about the roles of different hippocampal subfields in supporting this item–context binding. To address this question, we constructed a task in which items were affiliated with differing types of context—cognitive associations that vary at the local, item level and membership in temporally organized lists that linked items together at a global level. Participants made item recognition judgments while undergoing high-resolution fMRI. We performed voxel pattern similarity analyses to answer the question of how human hippocampal subfields represent retrieved information about cognitive states and the time at which a past event took place. As participants recollected previously presented items, activity patterns in the CA23DG subregion carried information about prior cognitive states associated with these items. We found no evidence to suggest reinstatement of information about temporal context at the level of list membership, but exploratory analyses revealed representations of temporal context at a coarse level in conjunction with representations of cognitive contexts. Results are consistent with characterizations of CA23DG as a critical site for binding together items and contexts in the service of memory retrieval.
Journal Articles
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Journal of Cognitive Neuroscience (2021) 33 (7): 1381–1395.
Published: 01 June 2021
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Studies have shown that transcranial direct current stimulation increases neuronal excitability of the targeted region and general connectivity of relevant functional networks. However, relatively little is understood of how the stimulation affects the connectivity relationship of the target with regions across the network structure of the brain. Here, we investigated the effects of transcranial direct current stimulation on the functional connectivity of the targeted region using resting-state fMRI scans of the human brain. Anodal direct current stimulation was applied to the left dorsolateral prefrontal cortex (lDLPFC; cathode on the right bicep), which belongs to the frontoparietal control network (FPCN) and is commonly targeted for neuromodulation of various cognitive functions including short-term memory, long-term memory, and cognitive control. lDLPFC's connectivity characteristics were quantified as graph theory measures, from the resting-state fMRI scans obtained prior to and following the stimulation. Critically, we tested pre- to poststimulation changes of the lDLPFC connectivity metrics following an active versus sham stimulation. We found that the stimulation had two distinct effects on the connectivity of lDLPFC: for Brodmann's area (BA) 9, it increased the functional connectivity between BA 9 and other nodes within the FPCN; for BA 46, net connectivity strength was not altered within FPCN, but connectivity distribution across networks (participation coefficient) was decreased. These findings provide insights that the behavioral changes as the functional consequences of stimulation may come about because of the increased role of lDLPFC in the FPCN.
Journal Articles
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Journal of Cognitive Neuroscience (2020) 32 (11): 2117–2130.
Published: 01 November 2020
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Prior studies demonstrated that neural oscillations are enhanced during working memory (WM) maintenance and that this activity can predict behavioral performance in healthy individuals. However, it is unclear whether the relationship holds for people with WM deficits. People with schizophrenia have marked WM deficits, and such deficits are most prominent when patients are required to process relationships between items, such as temporal order. Here, we used EEG to compare the relationship between oscillatory activity and WM performance in patients and controls. EEG was recorded as participants performed tasks requiring maintenance of complex objects (“Item”) or the temporal order of objects (“Order”). In addition to testing for group differences, we examined individual differences in EEG power and WM performance across groups. Behavioral results demonstrated that patients showed impaired performance on both Item and Order trials. EEG analyses revealed that patients showed an overall reduction in alpha power, but the relationship between alpha activity and performance was preserved. In contrast, patients showed a reduction in theta power specific to Order trials, and theta power could predict performance on Order trials in controls, but not in patients. These findings demonstrate that WM impairments in patients may reflect two different processes: a general deficit in alpha oscillations and a specific deficit in theta oscillations when temporal order information must be maintained. At a broader level, the results highlight the value of characterizing brain–behavior relationships, by demonstrating that the relationship between neural oscillations and WM performance can be fundamentally disrupted in those with WM deficits.
Journal Articles
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Journal of Cognitive Neuroscience (2019) 31 (1): 24–35.
Published: 01 January 2019
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Episodic memory is known to rely on the hippocampus, but how the hippocampus organizes different episodes to permit their subsequent retrieval remains controversial. One major area of debate hinges on a discrepancy between two hypothesized roles of the hippocampus: differentiating between similar events to reduce interference and assigning similar representations to events that share overlapping items and contextual information. Here, we used multivariate analyses of activity patterns measured with fMRI to characterize how the hippocampus distinguishes between memories based on similarity at the level of items and/or context. Hippocampal activity patterns discriminated between events that shared either item or context information but generalized across events that shared similar item–context associations. The current findings provide evidence that, whereas the hippocampus can reduce mnemonic interference by separating events that generalize along a single attribute dimension, overlapping hippocampal codes may support memory for events with overlapping item–context relations. This lends new insights into the way the hippocampus may balance multiple mnemonic operations in adaptively guiding behavior.
Journal Articles
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Journal of Cognitive Neuroscience (2018) 30 (11): 1646–1656.
Published: 01 November 2018
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Events that violate predictions are thought to not only modulate activity within the hippocampus and PFC but also enhance communication between the two regions. Scalp and intracranial EEG studies have shown that oscillations in the theta frequency band are enhanced during processing of contextually unexpected information. Some theories suggest that the hippocampus and PFC interact during processing of unexpected events, and it is possible that theta oscillations may mediate these interactions. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and PFC from two patients undergoing presurgical evaluation for pharmacoresistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal–prefrontal theta phase synchronization was significantly higher during encoding of contextually unexpected study items, relative to contextually expected study items. Furthermore, the hippocampal–prefrontal theta phase synchronization was larger for contextually unexpected items that were later remembered compared with later forgotten items. Moreover, we did not find increased theta synchronization between the PFC and rhinal cortex, suggesting that the observed effects were specific to prefrontal–hippocampal interactions. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and PFC in support of enhanced encoding of contextually deviant information.
Journal Articles
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Journal of Cognitive Neuroscience (2018) 30 (5): 667–679.
Published: 01 May 2018
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People can employ adaptive strategies to increase the likelihood that previously encoded information will be successfully retrieved. One such strategy is to constrain retrieval toward relevant information by reimplementing the neurocognitive processes that were engaged during encoding. Using EEG, we examined the temporal dynamics with which constraining retrieval toward semantic versus nonsemantic information affects the processing of new “foil” information encountered during a memory test. Time–frequency analysis of EEG data acquired during an initial study phase revealed that semantic compared with nonsemantic processing was associated with alpha decreases in a left frontal electrode cluster from around 600 msec after stimulus onset. Successful encoding of semantic versus nonsemantic foils during a subsequent memory test was related to decreases in alpha oscillatory activity in the same left frontal electrode cluster, which emerged relatively late in the trial at around 1000–1600 msec after stimulus onset. Across participants, left frontal alpha power elicited by semantic processing during the study phase correlated significantly with left frontal alpha power associated with semantic foil encoding during the memory test. Furthermore, larger left frontal alpha power decreases elicited by semantic foil encoding during the memory test predicted better subsequent semantic foil recognition in an additional surprise foil memory test, although this effect did not reach significance. These findings indicate that constraining retrieval toward semantic information involves reimplementing semantic encoding operations that are mediated by alpha oscillations and that such reimplementation occurs at a late stage of memory retrieval, perhaps reflecting additional monitoring processes.
Journal Articles
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Journal of Cognitive Neuroscience (2016) 28 (7): 1010–1023.
Published: 01 July 2016
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The human ventral temporal cortex (VTC) plays a critical role in object recognition. Although it is well established that visual experience shapes VTC object representations, the impact of semantic and contextual learning is unclear. In this study, we tracked changes in representations of novel visual objects that emerged after learning meaningful information about each object. Over multiple training sessions, participants learned to associate semantic features (e.g., “made of wood,” “floats”) and spatial contextual associations (e.g., “found in gardens”) with novel objects. fMRI was used to examine VTC activity for objects before and after learning. Multivariate pattern similarity analyses revealed that, after learning, VTC activity patterns carried information about the learned contextual associations of the objects, such that objects with contextual associations exhibited higher pattern similarity after learning. Furthermore, these learning-induced increases in pattern information about contextual associations were correlated with reductions in pattern information about the object's visual features. In a second experiment, we validated that these contextual effects translated to real-life objects. Our findings demonstrate that visual object representations in VTC are shaped by the knowledge we have about objects and show that object representations can flexibly adapt as a consequence of learning with the changes related to the specific kind of newly acquired information.
Journal Articles
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Journal of Cognitive Neuroscience (2014) 26 (8): 1694–1704.
Published: 01 August 2014
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Episodic memory is associated with the encoding and retrieval of context information and with a subjective sense of reexperiencing past events. The neural correlates of episodic retrieval have been extensively studied using fMRI, leading to the identification of a “general recollection network” including medial temporal, parietal, and prefrontal regions. However, in these studies, it is difficult to disentangle the effects of context retrieval from recollection. In this study, we used fMRI to determine the extent to which the recruitment of regions in the recollection network is contingent on context reinstatement. Participants were scanned during a cued recognition test for target words from encoded sentences. Studied target words were preceded by either a cue word studied in the same sentence (thus congruent with encoding context) or a cue word studied in a different sentence (thus incongruent with encoding context). Converging fMRI results from independently defined ROIs and whole-brain analysis showed regional specificity in the recollection network. Activity in hippocampus and parahippocampal cortex was specifically increased during successful retrieval following congruent context cues, whereas parietal and prefrontal components of the general recollection network were associated with confident retrieval irrespective of contextual congruency. Our findings implicate medial temporal regions in the retrieval of semantic context, contributing to, but dissociable from, recollective experience.
Journal Articles
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Journal of Cognitive Neuroscience (2014) 26 (5): 1085–1099.
Published: 01 May 2014
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Neural systems may be characterized by measuring functional interactions in the healthy brain, but it is unclear whether components of systems defined in this way share functional properties. For instance, within the medial temporal lobes (MTL), different subregions show different patterns of cortical connectivity. It is unknown, however, whether these intrinsic connections predict similarities in how these regions respond during memory encoding. Here, we defined brain networks using resting state functional connectivity (RSFC) then quantified the functional similarity of regions within each network during an associative memory encoding task. Results showed that anterior MTL regions affiliated with a network of anterior temporal cortical regions, whereas posterior MTL regions affiliated with a network of posterior medial cortical regions. Importantly, these connectivity relationships also predicted similarities among regions during the associative memory task. Both in terms of task-evoked activation and trial-specific information carried in multivoxel patterns, regions within each network were more similar to one another than were regions in different networks. These findings suggest that functional heterogeneity among MTL subregions may be related to their participation in distinct large-scale cortical systems involved in memory. At a more general level, the results suggest that components of neural systems defined on the basis of RSFC share similar functional properties in terms of recruitment during cognitive tasks and information carried in voxel patterns.
Journal Articles
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Journal of Cognitive Neuroscience (2014) 26 (4): 792–809.
Published: 01 April 2014
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Perceptual judgments can be based on two kinds of information: state-based perception of specific, detailed visual information, or strength-based perception of global or relational information. State-based perception is discrete in the sense that it either occurs or fails, whereas strength-based perception is continuously graded from weak to strong. The functional characteristics of these types of perception have been examined in some detail, but whether state- and strength-based perception are supported by different brain regions has been largely unexplored. A consideration of empirical work and recent theoretical proposals suggests that parietal and occipito-temporal regions may be differentially associated with state- and strength-based signals, respectively. We tested this parietal/occipito-temporal state/strength hypothesis using fMRI and a visual perception task that allows separation of state- and strength-based perception. Participants made same/different judgments on pairs of faces and scenes using a 6-point confidence scale where “6” responses indicated a state of perceiving specific details that had changed, and “1” to “5” responses indicated judgments based on varying strength of relational match/mismatch. Regions in the lateral and medial posterior parietal cortex (supramarginal gyrus, posterior cingulate cortex, and precuneus) were sensitive to state-based perception and were not modulated by varying levels of strength-based perception. In contrast, bilateral fusiform gyrus activation was increased for strength-based “different” responses compared with misses and did not show state-based effects. Finally, the lateral occipital complex showed increased activation for state-based responses and additionally showed graded activation across levels of strength-based perception. These results offer support for a state/strength distinction between parietal and temporal regions, with the lateral occipital complex at the intersection of state- and strength-based processing.
Journal Articles
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Journal of Cognitive Neuroscience (2011) 23 (1): 257–265.
Published: 01 January 2011
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Results from fMRI have strongly supported the idea that the ventrolateral PFC (VLPFC) contributes to successful memory formation, but the role the dorsolateral PFC (DLPFC) in memory encoding is more controversial. Some findings suggest that the DLPFC is recruited when one is processing relationships between items in working memory, and this processing specifically promotes subsequent memory for these relationships. However, previous studies could not rule out the possibility that DLPFC promotes memory during all elaborative encoding conditions and contributes to memory on all subsequent associative memory tests. To address this question directly, we used fMRI to examine activity during two encoding tasks that prompted participants to encode either relational or item-specific information. On relational trials, participants imagined pairs of items interacting, whereas on item-specific trials, participants imagined the items spatially separated and in different sizes. After scanning, we examined memory for relational information and item-specific information. fMRI results showed that DLPFC activity specifically promoted memory for relational information during relational encoding and not memory for item-specific information during item-specific encoding. In contrast, activity in the VLPFC predicted memory for both relational and item-specific information. The present results are consistent with the idea that the DLPFC specifically contributes to successful memory formation through its role in building relationships among items.
Journal Articles
Medial Temporal Lobe Activity during Source Retrieval Reflects Information Type, not Memory Strength
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Journal of Cognitive Neuroscience (2010) 22 (8): 1808–1818.
Published: 01 August 2010
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The medial temporal lobes (MTLs) are critical for episodic memory but the functions of MTL subregions are controversial. According to memory strength theory, MTL subregions collectively support declarative memory in a graded manner. In contrast, other theories assert that MTL subregions support functionally distinct processes. For instance, one view is that perirhinal cortex (PRc) processes item information, parahippocampal cortex (PHc) processes context information, and the hippocampus binds item and context. Here, we report two experiments that tested competing predictions from these models. In these studies, subjects encoded color–word associations by imagining color either as a contextual association (context detail condition) or as a feature of the item to be encoded (item detail condition). Results showed that encoding color information as an item detail improved source recognition in amnesic patients with recollection deficits. Furthermore, event-related fMRI data from healthy subjects revealed PRc activation associated with successful retrieval of item details, whereas activation in the hippocampus and PHc was associated with recollection-based source retrieval. The qualitatively different patterns of results observed in PRc and hippocampus/PHc are inconsistent with a memory strength account and are consistent with the idea that different MTL regions process different types of episodic information.
Journal Articles
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Journal of Cognitive Neuroscience (2007) 19 (3): 493–512.
Published: 01 March 2007
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The present study investigated the neurophysiological processes underlying associative long-term memory retrieval of objects and spatial positions by means of a modified fan paradigm with cued recall and two neuroimaging methods (electroencephalogram [EEG] and functional magnetic resonance imaging). In an acquisition phase, either one stimulus or two stimuli became associated with a noun. During retrieval, probe stimuli comprising noun pairs were presented, and participants had to recall the respective associations and decided whether the nouns are linked to each other via a commonly associated stimulus. With this design, the quality and quantity of recalled associations was systematically varied, whereas the triggering stimuli and response requirements were held constant in all experimental conditions. Recall time proved to be directly related to the number of associations fanning out from a retrieval cue. Correspondingly, the hemodynamic response (blood oxygen level-dependent [BOLD] signal) and the amplitude of slow negative EEG potentials increased monotonically with the number of associations in both left anterior and bilateral posterior cortical areas. These effects were consistently observed with content-specific topographies for the two distinct materials. Furthermore, the multimethod approach revealed a close temporal link between response times and event-related slow potential changes on the one side and a close topographical and amplitude correspondence between slow potentials and BOLD signal changes on the other. The integrated results suggest that the neuronal dynamics of associative memory retrieval are equivalent for different types of associations, but that the structural basis is clearly content-specific.
Journal Articles
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Journal of Cognitive Neuroscience (2006) 18 (3): 418–429.
Published: 01 March 2006
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Changes in memory function in elderly individuals are often attributed to dysfunction of the prefrontal cortex (PFC). One mechanism for this dysfunction may be disruption of white matter tracts that connect the PFC with its anatomical targets. Here, we tested the hypothesis that white matter degeneration is associated with reduced prefrontal activation. We used white matter hyperintensities (WMH), a magnetic resonance imaging (MRI) finding associated with cerebrovascular disease in elderly individuals, as a marker for white matter degeneration. Specifically, we used structural MRI to quantify the extent of WMH in a group of cognitively normal elderly individuals and tested whether these measures were predictive of the magnitude of prefrontal activity (fMRI) observed during performance of an episodic retrieval task and a verbal working memory task. We also examined the effects of WMH located in the dorsolateral frontal regions with the hypothesis that dorsal PFC WMH would be strongly associated with not only PFC function, but also with areas that are anatomically and functionally linked to the PFC in a task-dependent manner. Results showed that increases in both global and regional dorsal PFC WMH volume were associated with decreases in PFC activity. In addition, dorsal PFC WMH volume was associated with decreased activity in medial temporal and anterior cingulate regions during episodic retrieval and decreased activity in the posterior parietal and anterior cingulate cortex during working memory performance. These results suggest that disruption of white matter tracts, especially within the PFC, may be a mechanism for age-related changes in memory functioning.
Journal Articles
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Journal of Cognitive Neuroscience (2006) 18 (1): 33–47.
Published: 01 January 2006
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Numerous behavioral studies have suggested that normal aging has deleterious effects on episodic memory and that recollection is disproportionately impaired relative to familiarity-based recognition. However, there is a wide degree of variability in memory performance within the aging population and this generalization may not apply to all elderly adults. Here we investigated these issues by using event-related potentials (ERPs) to measure the effects of aging on the neural correlates of recollection and familiarity in older adults with recognition memory performance that was equivalent to (old-high) or lower than (old-low) that of young adults. Results showed that, behaviorally, old-high subjects exhibited intact recollection but reduced familiarity, whereas old-low subjects had impairments in both recollection and familiarity, relative to the young. Consistent with behavioral results, old-high subjects exhibited ERP correlates of recollection that were topographically similar to those observed in young subjects. However, unlike the young adults, old-high subjects did not demonstrate any neural correlates of familiarity-based recognition. In contrast to the old-high group, the old-low group exhibited neural correlates of recollection that were topographically distinct from those of the young. Our results suggest that the effects of aging on the underlying brain processes related to recollection and familiarity are dependent on individual memory performance and highlight the importance of examining performance variability in normal aging.
Journal Articles
Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence
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Journal of Cognitive Neuroscience (2005) 17 (7): 994–1010.
Published: 01 July 2005
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Theories of human memory have led to conflicting views regarding the relationship between working memory (WM) maintenance and episodic long-term memory (LTM) formation. Here, we tested the prediction that WM maintenance operates in two stages, and that processing during the initial stage of WM maintenance promotes successful LTM formation. Results from a functional magnetic resonance imaging study showed that activity in the dorsolateral prefrontal cortex and hippocampus during the initial stage of WM maintenance was predictive of subsequent LTM performance. In a behavioral experiment, we demonstrated that interfering with processing during the initial stage of WM maintenance impaired LTM formation. These results demonstrate that processing during the initial stage of WM maintenance directly contributes to successful LTM formation, and that this effect is mediated by a network that includes the dorsolateral prefrontal cortex and the hippocampus.
Journal Articles
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Journal of Cognitive Neuroscience (2004) 16 (6): 903–907.
Published: 01 July 2004
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Neuroimaging results have raised interest in characterizing hemispheric asymmetries in prefrontal activity during different types of memory retrieval tasks. In this issue, Dobbins et al. and Mitchell et al. report results suggesting that the two hemispheres of the prefrontal cortex may indeed make different contributions to memory retrieval. Here, I discuss these findings within the context of studies characterizing more general processing differences between the cerebral hemispheres and studies characterizing prefrontal organization along the dorsal– ventral and anterior–posterior dimensions.
Journal Articles
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Journal of Cognitive Neuroscience (1999) 11 (6): 598–609.
Published: 01 November 1999
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Previous neuropsychological and neuroimaging results have implicated the prefrontal cortex in memory retrieval, although its precise role is unclear. In the present study, we examined patterns of brain electrical activity during retrieval of episodic and semantic memories. In the episodic retrieval task, participants retrieved autobiographical memories in response to event cues. In the semantic retrieval task, participants generated exemplars in response to category cues. Novel sounds presented intermittently during memory retrieval elicited a series of brain potentials including one identifiable as the P3a potential. Based on prior research linking P3a with novelty detection and with the frontal lobes, we predicted that P3a would be reduced to the extent that novelty detection and memory retrieval interfere with each other. Results during episodic and semantic retrieval tasks were compared to results during a task in which subjects attended to the auditory stimuli. P3a amplitudes were reduced during episodic retrieval, particularly at right lateral frontal scalp locations. A similar but less lateralized pattern of frontal P3a reduction was observed during semantic retrieval. These findings support the notion that the right prefrontal cortex is engaged in the service of memory retrieval, particularly for episodic memories.