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).     

Role of parietal regions in episodic memory retrieval: the dual attentional processes hypothesis

Although parietal cortex is frequently activated during episodic memory retrieval, damage to this region does not markedly impair episodic memory. To account for these and other findings, a new dual attentional processes (DAP) hypothesis is proposed. According to this hypothesis, dorsal parietal cortex (DPC) contributes top-down attentional processes guided by retrieval goals, whereas ventral parietal cortex (VPC) contributes bottom-up attentional processes captured by the retrieval output. Consistent with this hypothesis, DPC activity increases with retrieval effort whereas VPC activity increases with confidence in old and new responses. The DAP hypothesis can also account for the overlap of parietal activations across different cognitive domains and for opposing effects of parietal activity on encoding vs. retrieval. Finally, the DAP hypothesis explains why VPC lesions yield a memory neglect syndrome: a deficit in spontaneously reporting relevant memory details but not in accessing the same details when guided by specific questions.     

Dissociable effects of top-down and bottom-up attention during episodic encoding

It is well established that the formation of memories for life's experiences-episodic memory-is influenced by how we attend to those experiences, yet the neural mechanisms by which attention shapes episodic encoding are still unclear. We investigated how top-down and bottom-up attention contribute to memory encoding of visual objects in humans by manipulating both types of attention during fMRI of episodic memory formation. We show that dorsal parietal cortex-specifically, intraparietal sulcus (IPS)-was engaged during top-down attention and was also recruited during the successful formation of episodic memories. By contrast, bottom-up attention engaged ventral parietal cortex-specifically, temporoparietal junction (TPJ)-and was also more active during encoding failure. Functional connectivity analyses revealed further dissociations in how top-down and bottom-up attention influenced encoding: while both IPS and TPJ influenced activity in perceptual cortices thought to represent the information being encoded (fusiform/lateral occipital cortex), they each exerted opposite effects on memory encoding. Specifically, during a preparatory period preceding stimulus presentation, a stronger drive from IPS was associated with a higher likelihood that the subsequently attended stimulus would be encoded. By contrast, during stimulus processing, stronger connectivity with TPJ was associated with a lower likelihood the stimulus would be successfully encoded. These findings suggest that during encoding of visual objects into episodic memory, top-down and bottom-up attention can have opposite influences on perceptual areas that subserve visual object representation, suggesting that one manner in which attention modulates memory is by altering the perceptual processing of to-be-encoded stimuli.     

Cortical representations of personally familiar objects and places: functional organization of the human posterior cingulate cortex

The recognition of both personally familiar objects and places involves nonspatial memory retrieval processes, but only personally familiar places are represented as space. Although the posterior cingulate cortex (PCC) is considered to process both types of such memories, its functional organization is poorly understood. In this event-related fMRI study, normal subjects judged familiar/unfamiliar pictures in four categories: familiar places (FP), familiar objects (FO), unfamiliar places (UP), and unfamiliar objects (UO), thus constituting a two-factorial design. A significant main effect of stimuli with greater activation in the place (FP and UP) than object (FO and UO) trials was observed bilaterally in several medial temporo-occipito-parietal regions, including the caudal PCC (cPCC) and parahippocampal gyrus. The reverse comparison revealed greater activation in the lateral inferior occipito-temporal junctions and intraparietal sulci bilaterally. A significant main effect of familiarity with greater activation in the familiar (FP and FO) than unfamiliar (UP and UO) trials was observed in the mid-dorsal PCC (mPCC), retrosplenial cortex, posterior precuneus, and the left intraparietal sulcus. Activation specific to the FP trials (as assessed by the interaction) was observed in the right posterodorsal PCC (pPCC) only. Together with data from previous functional imaging studies, the results suggest a functional segregation of human PCC with differential involvement of pPCC in spatial representations of personally familiar places and of the mPCC and retrosplenial cortex in episodic retrieval of personally familiar places and objects. Activation of the left intraparietal sulcus may reflect retrieval of memories related to object manipulation.     

The neural correlates of recollection: hippocampal activation declines as episodic memory fades

Memories for certain events tend to linger in rich, vivid detail, and retrieval of these memories includes a sense of re-experiencing the details of the event. Most events, however, are not retained in any detailed way for more than a few days. According to one theory, the hippocampus plays a specific role in supporting episodic retrieval, that is, the re-experiencing of an event as part of one's personal past. This theory predicts that as episodic memories fade over time and are reduced to feelings of familiarity, activity in the hippocampus should no longer be associated with retrieval. We used high-resolution functional imaging to explore neural activity in medial temporal lobe subregions while participants performed a recognition task at both a short (10-min) and long (1-week) study-test delay. For each recognized item, subjects made "Remember/Know" judgments, allowing us to distinguish between items that were consistently episodic across the two tests and items that were initially episodic, but later became merely familiar. Our results demonstrate that activity in the subiculum is specifically associated with episodic recollection. Overall, recollected items were associated with higher activity in the subiculum than other items. For transiently recollected items, there was a decrease in subicular activity across the 1-week delay as memory faded from recollection to familiarity, whereas consistently recollected items were associated with enhanced subicular activity at both delays. These results provide evidence of a link between subicular activation and recollective experience.     

Brain areas specific for attentional load in a motion-tracking task.

Although visual attention is known to modulate brain activity in the posterior parietal, prefrontal, and visual sensory areas, the unique roles of these areas in the control of attentional resources have remained unclear. Here, we report a dissociation in the response profiles of these areas. In a parametric functional magnetic resonance imaging (fMRI) study, subjects performed a covert motion-tracking task, in which we manipulated "attentional load" by varying the number of tracked balls. While strong effects of attention--independent of attentional load--were widespread, robust linear increases of brain activity with number of balls tracked were seen primarily in the posterior parietal areas, including the intraparietal sulcus (IPS) and superior parietal lobule (SPL). Thus, variations in attentional load revealed different response profiles in sensory areas as compared to control areas. Our results suggest a general role for posterior parietal areas in the deployment of visual of attentional resources.     

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.     

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.     

The neural correlates of attention orienting in visuospatial working memory for detecting feature and conjunction changes

The neural mechanisms of attentional orienting in visuospatial working memory for change detection were investigated. A spatial cue was provided with the onset time manipulated to allow more effective top-down control with an early cue than with a late cue. The change type was also manipulated so that accurate detection depended on color or the binding of color and location. The results showed that both the frontal and parietal regions subserved the change detection task without cueing. When data were collapsed over the two change types, early cueing increased activation in the right inferior frontal gyrus (IFG) and middle frontal gyrus (MFG) while late cueing increased activation in the right inferior parietal lobule (IPL) and temporoparietal junction (TPJ) as compared with the no-cue condition. The cue onset time led to different levels of enhancement in the frontal and posterior cortices related to top-down control and stimulus-driven orienting. For feature detection, early cueing increased activation in the right MFG and late cueing increased activation in the bilateral precuneus (PCu), right TPJ, and right cuneus. The neural correlates of conjunction detection involved the right PCu and cerebellum without cueing, were associated with the anterior MFG, left IFG, and the left STG with early cueing, and involved the right MFG, left IFG, and right IPL with late cueing. The left IFG was correlated with memory retrieval of the cued representation for conjunction detection, and the right posterior PCu was associated with maintenance and memory retrieval among competing stimuli.     

Impact of emotional salience on episodic memory in attention-deficit/hyperactivity disorder: a functional magnetic resonance imaging study.

BACKGROUND: Patients with attention-deficit/hyperactivity disorder (ADHD) show episodic memory deficits especially in complex memory tasks. We investigated the neural correlates of memory formation in ADHD and their modulation by stimulus salience. METHODS: We recorded event-related functional magnetic resonance imaging during an episodic memory paradigm with neutral and emotional pictures in 12 male ADHD subjects and 12 healthy adolescents. RESULTS: Emotional salience did significantly augment memory performance in ADHD patients. Successful encoding of neutral pictures was associated with activation of the anterior cingulate cortex (ACC) in healthy adolescents but with activation of the superior parietal lobe (SPL) and precuneus in ADHD patients. Successful encoding of emotional pictures was associated with prefrontal and inferior temporal cortex activation in both groups. Healthy adolescents, moreover, showed deactivation in the inferior parietal lobe. CONCLUSIONS: From a pathophysiological point of view, the most striking functional differences between healthy adolescents and ADHD patients were in the ACC and SPL. We suggest that increased SPL activation in ADHD reflected attentional compensation for low ACC activation during the encoding of neutral pictures. The higher salience of emotional stimuli, in contrast, regulated the interplay between ACC and SPL in conjunction with improving memory to the level of healthy adolescents.     

The role of the left posterior parietal lobule in top-down modulation on space-based attention: a transcranial magnetic stimulation study

Converging evidence from neuroimaging as well as lesion and transcranial magnetic stimulation (TMS) studies has been obtained for the involvement of right ventral posterior parietal cortex (PPC) in exogenous orienting. However, the contribution of dorsal PPC to attentional orienting, particularly endogenous orienting, is still under debate. In an informative peripheral cueing paradigm, in which the exogenous and endogenous orienting can be studied in relative isolation within a single task, we applied TMS over sub-regions of dorsal PPC to explore their possible distinct involvement in exogenous and endogenous processes. We found that disruption of the left posterior intraparietal sulcus (pIPS) weakened the attentional effects of endogenous orienting, but did not affect exogenous processes. In addition, TMS applied over the right superior parietal lobule (SPL) resulted in an overall increase in reaction times. The present study provides the causal evidence that the left pIPS plays a crucial role in voluntary orienting of visual attention, while right SPL is involved in the processing of arousal and/or vigilance.     

Transient memory loss for people.

A patient had transient memory loss for close family members. She could not even recognise their names as familiar. Her everyday memory was relatively preserved and she retained a clear recollection of the episode. Standard and sleep deprived EEG showed a mild abnormality of the left temporal lobe. Neuropsychological testing found evidence for a mild verbal memory impairment. The findings provide further evidence for the fractionation of transient forms of amnesia, support the dissociation of semantic/retrograde amnesia from episodic/anterograde amnesia, and offer evidence in favour of a left temporal lobe site for retrieval of past memories relating to the identification of people.     

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.     

Cortical activation patterns during long-term memory retrieval of visually or haptically encoded objects and locations

The present study used functional magnetic resonance imaging to delineate cortical networks that are activated when objects or spatial locations encoded either visually (visual encoding group, n=10) or haptically (haptic encoding group, n=10) had to be retrieved from long-term memory. Participants learned associations between auditorily presented words and either meaningless objects or locations in a 3-D space. During the retrieval phase one day later, participants had to decide whether two auditorily presented words shared an association with a common object or location. Thus, perceptual stimulation during retrieval was always equivalent, whereas either visually or haptically encoded object or location associations had to be reactivated. Moreover, the number of associations fanning out from each word varied systematically, enabling a parametric increase of the number of reactivated representations. Recall of visual objects predominantly activated the left superior frontal gyrus and the intraparietal cortex, whereas visually learned locations activated the superior parietal cortex of both hemispheres. Retrieval of haptically encoded material activated the left medial frontal gyrus and the intraparietal cortex in the object condition, and the bilateral superior parietal cortex in the location condition. A direct test for modality-specific effects showed that visually encoded material activated more vision-related areas (BA 18/19) and haptically encoded material more motor and somatosensory-related areas. A conjunction analysis identified supramodal and material-unspecific activations within the medial and superior frontal gyrus and the superior parietal lobe including the intraparietal sulcus. These activation patterns strongly support the idea that code-specific representations are consolidated and reactivated within anatomically distributed cell assemblies that comprise sensory and motor processing systems.     

Common and unique neural activations in autobiographical, episodic, and semantic retrieval

This study sought to explore the neural correlates that underlie autobiographical, episodic, and semantic memory. Autobiographical memory was defined as the conscious recollection of personally relevant events, episodic memory as the recall of stimuli presented in the laboratory, and semantic memory as the retrieval of factual information and general knowledge about the world. Our objective was to delineate common neural activations, reflecting a functional overlap, and unique neural activations, reflecting functional dissociation of these memory processes. We conducted an event-related functional magnetic resonance imaging study in which we utilized the same pictorial stimuli but manipulated retrieval demands to extract autobiographical, episodic, or semantic memories. The results show a functional overlap of the three types of memory retrieval in the inferior frontal gyrus, the middle frontal gyrus, the caudate nucleus, the thalamus, and the lingual gyrus. All memory conditions yielded activation of the left medial-temporal lobe; however, we found a functional dissociation within this region. The anterior and superior areas were active in episodic and semantic retrieval, whereas more posterior and inferior areas were active in autobiographical retrieval. Unique activations for each memory type were also delineated, including medial frontal increases for autobiographical, right middle frontal increases for episodic, and right inferior temporal increases for semantic retrieval. These findings suggest a common neural network underlying all declarative memory retrieval, as well as unique neural contributions reflecting the specific properties of retrieved memories.     

The development of control processes supporting source memory discrimination as revealed by event-related potentials

Improvement in source memory performance throughout childhood is thought to be mediated by the development of executive control. As postretrieval control processes may be better time-locked to the recognition response rather than the retrieval cue, the development of processes underlying source memory was investigated with both stimulus- and response-locked event-related potentials (ERPs). These were recorded in children, adolescents, and adults during a recognition memory exclusion task. Green- and red-outlined pictures were studied, but were tested in black outline. The test requirement was to endorse old items shown in one study color ("targets") and to reject new items along with old items shown in the alternative study color ("nontargets"). Source memory improved with age. All age groups retrieved target and nontarget memories as reflected by reliable parietal episodic memory (EM) effects, a stimulus-locked ERP correlate of recollection. Response-locked ERPs to targets and nontargets diverged in all groups prior to the response, although this occurred at an increasingly earlier time point with age. We suggest these findings reflect the implementation of attentional control mechanisms to enhance target memories and facilitate response selection with the greatest and least success, respectively, in adults and children. In adults only, response-locked ERPs revealed an early-onsetting parietal negativity for nontargets, but not for targets. This was suggested to reflect adults' ability to consistently inhibit prepotent target responses for nontargets. The findings support the notion that the development of source memory relies on the maturation of control processes that serve to enhance accurate selection of task-relevant memories.     

Brain regions associated with successful and unsuccessful retrieval of verbal episodic memory as revealed by divided attention

Which brain regions are implicated when words are retrieved under divided attention, and what does this tell us about attentional and memory processes needed for retrieval? To address these questions we used fMRI to examine brain regions associated with auditory recognition performed under full and divided attention (DA). We asked young adults to encode words presented auditorily under full attention (FA), and following this, asked them to recognize studied words while in the scanner. Attention was divided at retrieval by asking participants to perform either an animacy task to words, or odd-digit identification task to numbers presented visually, concurrently with the recognition task. Retrieval was disrupted significantly by the word-, but not number-based concurrent task. A corresponding decrease in brain activity was observed in right hippocampus, bilateral parietal cortex, and left precuneus, thus demonstrating, for the first time, involvement of these regions in recognition under DA at retrieval. Increases in activation of left prefrontal cortex (PFC), associated with phonological processing, were observed in the word- compared to number-based DA condition. Results suggest that the medial temporal lobe (MTL) and neo-cortical components of retrieval, believed to form the basis of episodic memory traces, are disrupted when phonological processing regions in left PFC are engaged simultaneously by another task. Results also support a component-process model of retrieval which posits that MTL-mediated retrieval does not compete for general cognitive resources but does compete for specific structural representations.     

Spatial attention deficits in humans: the critical role of superior compared to inferior parietal lesions

According to a longstanding view, inferior as opposed to superior parietal cortex critically contributes to the spatial attentional deficits encountered following unilateral parietal ischemic lesions. We review the evidence on which this view is based and contrast it with more recent structural lesion evidence concerning the critical role of the intraparietal sulcus in spatial attention deficits. In a classical spatial cueing paradigm, focal lesions of the posterior and of the middle segment of the intraparietal sulcus give rise to a pathological invalidity effect that is indistinguishable from that seen after classical inferior parietal lesions. When a competing distracter is added to a target stimulus, the deleterious consequences of focal IPS lesions are again very similar to those classically observed following inferior parietal lesions. The deficit could not be accounted for by functional effects at a distance affecting inferior parietal cortex. These single-case lesion data establish the critical role of the posterior and the middle IPS segment in spatially selective attention and are in line with a vast amount of functional imaging evidence in the intact brain pointing to the prominent role of the intraparietal sulcus in spatial attention, along with inferior parietal cortex under specific circumstances. Functional imaging has also provided hints about the differences in functional contribution between inferior and superior parietal cortex. These hypotheses await further confirmation based on lesion evidence.     

Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task

Subjects were required to navigate through a virtual 3D labyrinth presented on a screen while fMRI images were obtained. Contrasting the fMRI images obtained during the navigation trials with appropriate control conditions revealed a bilateral network comprising the parietal lobe (including the intraparietal sulcus) and various lateral and medial premotor areas. The subjects using an allocentric strategy showed stronger activation in the medial temporal areas including the parahippocampal region, the hippocampus, and the thalamus. In addition, the cerebellum was also active in those subjects. We believe that this activation pattern is related to visually guided memory retrieval based on generalized spatial maps. The stronger activation in the thalamic-basal ganglia-cerebellar-loop points to a more automatic support of memory and attentional processes possibly supporting memorization of spatial maps.     

Neural activity associated with episodic memory for emotional context

To address the question of which brain regions subserve retrieval of emotionally-valenced memories, we used event-related fMRI to index neural activity during the incidental retrieval of emotional and non-emotional contextual information. At study, emotionally neutral words were presented in the context of sentences that were either negatively, neutrally or positively valenced. At test, fMRI data were obtained while participants discriminated between studied and unstudied words. Recognition of words presented in emotionally negative relative to emotionally neutral contexts was associated with enhanced activity in right dorsolateral prefrontal cortex, left amygdala and hippocampus, right lingual gyrus and posterior cingulate cortex. Recognition of words from positive relative to neutral contexts was associated with increased activity in bilateral prefrontal and orbitofrontal cortices, and left anterior temporal lobe. These findings suggest that neural activity mediating episodic retrieval of contextual information and its subsequent processing is modulated by emotion in at least two ways. First, there is enhancement of activity in networks supporting episodic retrieval of neutral information. Second, regions known to be activated when emotional information is encountered in the environment are also active when emotional information is retrieved from memory.