Overlapping parietal activity in memory and perception: evidence for the attention to memory model

The specific role of different parietal regions to episodic retrieval is a topic of intense debate. According to the Attention to Memory (AtoM) model, dorsal parietal cortex (DPC) mediates top-down attention processes guided by retrieval goals, whereas ventral parietal cortex (VPC) mediates bottom-up attention processes captured by the retrieval output or the retrieval cue. This model also hypothesizes that the attentional functions of DPC and VPC are similar for memory and perception. To investigate this last hypothesis, we scanned participants with event-related fMRI whereas they performed memory and perception tasks, each comprising an orienting phase (top-down attention) and a detection phase (bottom-up attention). The study yielded two main findings. First, consistent with the AtoM model, orienting-related activity for memory and perception overlapped in DPC, whereas detection-related activity for memory and perception overlapped in VPC. The DPC overlap was greater in the left intraparietal sulcus, and the VPC overlap in the left TPJ. Around overlapping areas, there were differences in the spatial distribution of memory and perception activations, which were consistent with trends reported in the literature. Second, both DPC and VPC showed stronger connectivity with medial-temporal lobe during the memory task and with visual cortex during the perception task. These findings suggest that, during memory tasks, some parietal regions mediate similar attentional control processes to those involved in perception tasks (orienting in DPC vs. detection in VPC), although on different types of information (mnemonic vs. sensory).     

Episodic autobiographical memory in amnestic mild cognitive impairment: What are the neural correlates?

Autobiographical memory in amnestic Mild Cognitive Impairment (aMCI) is characterized by impaired retrieval of episodic memories, but relatively preserved personal semantic knowledge. This study aimed to identify (via FDG‐PET) the neural substrates of impaired episodic specificity of autobiographical memories in 35 aMCI patients compared with 24 healthy elderly controls. Significant correlations between regional cerebral activity and the proportion of episodic details in autobiographical memories from two life periods were found in specific regions of an autobiographical brain network. In aMCI patients, more than in controls, specifically episodic memories from early adulthood were associated with metabolic activity in the cuneus and in parietal regions. We hypothesized that variable retrieval of episodic autobiographical memories in our aMCI patients would be related to their variable capacity to reactivate specific sensory‐perceptual and contextual details of early adulthood events linked to reduced (occipito‐parietal) visual imagery and less efficient (parietal) attentional processes. For recent memories (last year), a correlation emerged between the proportion of episodic details and activity in lateral temporal regions and the temporo‐parietal junction. Accordingly, variable episodic memory for recent events may be related to the efficiency of controlled search through general events likely to provide cues for the retrieval of episodic details and to the ability to establish a self perspective favouring recollection. Hum Brain Mapp, 2013. © 2012 Wiley Periodicals, Inc.     

Early parietal response in episodic retrieval revealed with MEG

Recent neuroimaging and lesion studies have led to competing hypotheses for potential roles of the left lateral parietal lobe in episodic memory retrieval. These hypotheses may be dissociated by whether they imply a role in preretrieval or postretrieval processes. For example, one hypothesis is the left parietal cortex (particularly in more ventral subregions) forms part of an “episodic buffer” that supports the online representation of the retrieved target, a role that is, by definition, postretrieval. An alternate view maintains parietal activity (particularly in more dorsal subregions) contributes to top‐down orientation of attention to retrieval search, a preretrieval role. The present investigation seeks to reveal the earliest onset of lateral parietal activity in three anatomically‐defined subregions of the left lateral parietal cortex to identify any preretrieval activation. Subjects performed a pair‐cued recall task while neural activity was recorded with magnetoencephalography (MEG) at millisecond temporal resolution. MEG data were then mapped to each subject's cortical surface using dynamic statistical parametric mapping (dSPM). Both dorsal and ventral regions showed retrieval‐related activations beginning within ～100 ms of the cue to retrieve and lasting up to 400 ms. We conclude that this early and transient pattern of activity in lateral parietal cortex is most consistent with a preretrieval role, possibly in directing attention to episodic memory retrieval. Hum Brain Mapp, 2011. © 2010 Wiley‐Liss, Inc.     

Top-down and bottom-up attention to memory: a hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval

Recent neuroimaging studies have implicated the posterior parietal cortex in episodic memory retrieval, but there is uncertainty about its specific role. Research in the attentional domain has shown that superior parietal lobe (SPL) regions along the intraparietal sulcus are implicated in the voluntary orienting of attention to relevant aspects of the environment, whereas inferior parietal lobe (IPL) regions at the temporo-parietal junction mediate the automatic allocation of attention to task-relevant information. Here we propose that the SPL and the IPL play conceptually similar roles in episodic memory retrieval. We hypothesize that the SPL allocates top-down attention to memory retrieval, whereas the IPL mediates the automatic, bottom-up attentional capture by retrieved memory contents. By reviewing the existing fMRI literature, we show that the posterior intraparietal sulcus of SPL is consistently active when the need for top-down assistance to memory retrieval is supposedly maximal, e.g., for memories retrieved with low vs. high confidence, for familiar vs. recollected memories, for recognition of high vs. low frequency words. On the other hand, the supramarginal gyrus of IPL is consistently active when the attentional capture by memory contents is supposedly maximal, i.e., for strong vs. weak memories, for vividly recollected vs. familiar memories, for memories retrieved with high vs. low confidence. We introduce a model of episodic memory retrieval that characterizes contributions of posterior parietal cortex.     

Neural correlates of confidence during item recognition and source memory retrieval: evidence for both dual-process and strength memory theories

Although the medial-temporal lobes (MTL), PFC, and parietal cortex are considered primary nodes in the episodic memory network, there is much debate regarding the contributions of MTL, PFC, and parietal subregions to recollection versus familiarity (dual-process theory) and the feasibility of accounts on the basis of a single memory strength process (strength theory). To investigate these issues, the current fMRI study measured activity during retrieval of memories that differed quantitatively in terms of strength (high vs. low-confidence trials) and qualitatively in terms of recollection versus familiarity (source vs. item memory tasks). Support for each theory varied depending on which node of the episodic memory network was considered. Results from MTL best fit a dual-process account, as a dissociation was found between a right hippocampal region showing high-confidence activity during the source memory task and bilateral rhinal regions showing high-confidence activity during the item memory task. Within PFC, several left-lateralized regions showed greater activity for source than item memory, consistent with recollective orienting, whereas a right-lateralized ventrolateral area showed low-confidence activity in both tasks, consistent with monitoring processes. Parietal findings were generally consistent with strength theory, with dorsal areas showing low-confidence activity and ventral areas showing high-confidence activity in both tasks. This dissociation fits with an attentional account of parietal functions during episodic retrieval. The results suggest that both dual-process and strength theories are partly correct, highlighting the need for an integrated model that links to more general cognitive theories to account for observed neural activity during episodic memory retrieval.     

Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective

Although regions of the parietal cortex have been consistently implicated in episodic memory retrieval, the functional roles of these regions remain poorly understood. The present review presents a meta-analysis of findings from event-related fMRI studies reporting the loci of retrieval effects associated with familiarity- and recollection-related recognition judgments. The results of this analysis support previous suggestions that retrieval-related activity in lateral parietal cortex dissociates between superior regions, where activity likely reflects the task relevance of different classes of recognition test items, and more inferior regions where retrieval-related activity appears closely linked to successful recollection. It is proposed that inferior lateral parietal cortex forms part of a neural network supporting the 'episodic buffer' [Baddeley, A. D. (2000). The episodic buffer: A new component of working memory? Trends in Cognitive Sciences, 4, 417-423].     

Dissociating the “retrieval success” regions of the brain: Effects of retrieval delay

There is abundant evidence that the hippocampal formation critically supports episodic memory retrieval, the remembering of episodes including contextual details. Yet, a group of other brain regions has also been consistently implicated in successful episodic retrieval. This retrieval success network (RSN) includes the posterior midline region, medial prefrontal cortex (mPFC), and posterior parietal cortex (PPC). Despite these consistent findings, the functional roles of the RSN regions remain poorly understood. Given that vivid remembering leads to high-confidence retrieval decisions, it is unclear whether activity in these regions reflects episodic long-term memory, or is merely associated with retrieval confidence. In order to distinguish between these alternatives, we manipulated study-test delays within the context of a continuous recognition task during fMRI-scanning. The design was based on previous evidence indicating that retrieval at short delays is easier leading to high-evidence mnemonic decisions, whereas retrieval at longer delays is more difficult but also more hippocampus-dependent. Confirming previous findings, we found that retrieval decisions at short delays were more accurate and faster, and that the hippocampus showed greater activity at longer delays. Within the other RSN regions, we found three distinct activation patterns as a function of delay. Similar to the hippocampus, the retrosplenial cortex showed increased activity as a function of retrieval delay. Dorsal PPC and the precuneus showed decreased activity. Finally, the posterior cingulate, medial PFC and ventral PPC showed a V-shaped pattern. These findings support the idea that dorsal PPC and the precuneus are involved in decision-related retrieval processes rather than successful remembering.     

Sustained and transient neural modulations in prefrontal cortex related to declarative long-term memory, working memory, and attention

Common activations in prefrontal cortex (PFC) during episodic and semantic long-term memory (LTM) tasks have been hypothesized to reflect functional overlap in terms of working memory (WM) and cognitive control. To evaluate a WM account of LTM-general activations, the present study took into consideration that cognitive task performance depends on the dynamic operation of multiple component processes, some of which are stimulus-synchronous and transient in nature; and some that are engaged throughout a task in a sustained fashion. PFC and WM may be implicated in both of these temporally independent components. To elucidate these possibilities we employed mixed blocked/event-related functional magnetic resonance imaging (fMRI) procedures to assess the extent to which sustained or transient activation patterns overlapped across tasks indexing episodic and semantic LTM, attention (ATT), and WM. Within PFC, ventrolateral and medial areas exhibited sustained activity across all tasks, whereas more anterior regions including right frontopolar cortex were commonly engaged in sustained processing during the three memory tasks. These findings do not support a WM account of sustained frontal responses during LTM tasks, but instead suggest that the pattern that was common to all tasks reflects general attentional set/vigilance, and that the shared WM-LTM pattern mediates control processes related to upholding task set. Transient responses during the three memory tasks were assessed relative to ATT to isolate item-specific mnemonic processes and were found to be largely distinct from sustained effects. Task-specific effects were observed for each memory task. In addition, a common item response for all memory tasks involved left dorsolateral PFC (DLPFC). The latter response might be seen as reflecting WM processes during LTM retrieval. Thus, our findings suggest that a WM account of shared PFC recruitment in LTM tasks holds for common transient item-related responses rather than sustained state-related responses that are better seen as reflecting more general attentional/control processes.     

Prefrontal and parietal cortex in human episodic memory: an interference study by repetitive transcranial magnetic stimulation

Neuroimaging findings, including repetitive transcranial magnetic stimulation (rTMS) interference, point to an engagement of prefrontal cortex (PFC) in learning and memory. Whether parietal cortex (PC) activity is causally linked to successful episodic encoding and retrieval is still uncertain. We compared the effects of event-related active or sham rTMS (a rapid-rate train coincident to the very first phases of memoranda presentation) to the left or right intraparietal sulcus, during a standardized episodic memory task of visual scenes, with those obtained in a fully matched sample of subjects who received rTMS on left or right dorsolateral PFC during the same task. In these subjects, specific hemispheric effects of rTMS included interference with encoding after left stimulation and disruption of retrieval after right stimulation. The interference of PC-rTMS on encoding/retrieval performance was negligible, lacking specificity even when higher intensities of stimulation were applied. However, right PC-rTMS of the same intensity lengthened reaction times in the context of a purely attentive visuospatial task. These results suggest that the activity of intraparietal sulci shown in several functional magnetic resonance studies on memory, unlike that of the dorsolateral PFC, is not causally engaged to a useful degree in memory encoding and retrieval of visual scenes. The parietal activations accompanying the memorization processes could reflect the engagement of a widespread brain attentional network, in which interference on a single 'node' is insufficient for an overt disruption of memory performance.     

fMRI correlates of retrieval orientation

Processes related to the cueing of memory retrieval were investigated using fMRI during a yes/no recognition memory test. Participants studied either pictures or auditory words and were subsequently tested with visual words that either corresponded to studied items (old items) or were unstudied (new items). It was expected that neural activity would differ according to the type of information participants are trying to retrieve: a manifestation of the so-called "retrieval orientation" effect. We replicated robust old/new effects in parietal, prefrontal and anterior medial temporal lobe cortices, which did not differ according to the study material. However, we did observe differential activity to test items in temporoparietal cortex and fusiform cortex as a function of the study material. More specifically, attempts to retrieve words encoded auditorily produced greater activity in auditory cortex than attempts to retrieve words encoded as pictures, whereas the converse was found in fusiform cortex. The above pattern was found for both new and old test items. These findings implicate these regions in constraining the search for specific types of encoded information and thus are in accordance with the transfer-appropriate processing framework. Further, we propose that our results can be seen as an extension of the cortical reinstatement hypothesis, in that the same material-specific cortical regions are engaged during both encoding and retrieval, and this increases the likelihood of successful recognition, or rejection, of retrieval cues in a memory test.