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).     

Deconstructing the architecture of dorsal and ventral attention systems with dynamic causal modeling

Attentional orientation to a spatial cue and reorientation-after invalid cueing-are mediated by two distinct networks in the human brain. A bilateral dorsal frontoparietal network, comprising the intraparietal sulcus (IPS) and the frontal eye fields (FEF), controls the voluntary deployment of attention and may modulate visual cortex in preparation for upcoming stimulation. In contrast, reorienting attention to invalidly cued targets engages a right-lateralized ventral frontoparietal network comprising the temporoparietal junction (TPJ) and ventral frontal cortex. The present fMRI study investigated the functional architecture of these two attentional systems by characterizing effective connectivity during lateralized orienting and reorienting of attention, respectively. Subjects performed a modified version of Posner's location-cueing paradigm. Dynamic causal modeling (DCM) of regional responses in the dorsal and ventral network, identified in a conventional (SPM) whole-brain analysis, was used to compare different functional architectures. Bayesian model selection showed that top-down connections from left and right IPS to left and right visual cortex, respectively, were modulated by the direction of attention. Moreover, model evidence was highest for a model with directed influences from bilateral IPS to FEF, and reciprocal coupling between right and left FEF. Invalid cueing enhanced forward connections from visual areas to right TPJ, and directed influences from right TPJ to right IPS and IFG (inferior frontal gyrus). These findings shed further light on the functional organization of the dorsal and ventral attentional network and support a context-sensitive lateralization in the top-down (backward) mediation of attentional orienting and the bottom-up (forward) effects of invalid cueing.     

Perceptual and Semantic Representations at Encoding Contribute to True and False Recognition of Objects

When encoding new episodic memories, visual and semantic processing is proposed to make distinct contributions to accurate memory and memory distortions. Here, we used fMRI and preregistered representational similarity analysis to uncover the representations that predict true and false recognition of unfamiliar objects. Two semantic models captured coarse-grained taxonomic categories and specific object features, respectively, while two perceptual models embodied low-level visual properties. Twenty-eight female and male participants encoded images of objects during fMRI scanning, and later had to discriminate studied objects from similar lures and novel objects in a recognition memory test. Both perceptual and semantic models predicted true memory. When studied objects were later identified correctly, neural patterns corresponded to low-level visual representations of these object images in the early visual cortex, lingual, and fusiform gyri. In a similar fashion, alignment of neural patterns with fine-grained semantic feature representations in the fusiform gyrus also predicted true recognition. However, emphasis on coarser taxonomic representations predicted forgetting more anteriorly in the anterior ventral temporal cortex, left inferior frontal gyrus and, in an exploratory analysis, left perirhinal cortex. In contrast, false recognition of similar lure objects was associated with weaker visual analysis posteriorly in early visual and left occipitotemporal cortex. The results implicate multiple perceptual and semantic representations in successful memory encoding and suggest that fine-grained semantic as well as visual analysis contributes to accurate later recognition, while processing visual image detail is critical for avoiding false recognition errors.SIGNIFICANCE STATEMENT People are able to store detailed memories of many similar objects. We offer new insights into the encoding of these specific memories by combining fMRI with explicit models of how image properties and object knowledge are represented in the brain. When people processed fine-grained visual properties in occipital and posterior temporal cortex, they were more likely to recognize the objects later and less likely to falsely recognize similar objects. In contrast, while object-specific feature representations in fusiform gyrus predicted accurate memory, coarse-grained categorical representations in frontal and temporal regions predicted forgetting. The data provide the first direct tests of theoretical assumptions about encoding true and false memories, suggesting that semantic representations contribute to specific memories as well as errors.     

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.     

Dissociation of attention and intention in human posterior parietal cortex: an fMRI study

In natural environments, the orienting of attention to an object of interest occurs jointly with selecting it as a potential target for action. This coupling of perceptual selection and motor planning has led to 'the premotor theory of attention', which argues that attention and intention share the same neural mechanism. Here we used fMRI to test this hypothesis by examining neural activity in the temporal parietal junction (TPJ) and intraparietal sulcus (IPS) of the posterior parietal cortex (PPC) while subjects searched for a target among distractors with the presence of color singletons. Task-relevant salience of stimuli and the variability of response time were used to characterize the behavior of attention and intention components of the visuomotor transformation performed in these two cortical regions, respectively. We found that TPJ responses were significantly higher when the color singletons were distractors (vs. targets), suggesting that the TPJ was involved in attentional control of interference from task-irrelevant but salient stimuli. In contrast, signals in the IPS were closely related to the variability of response time, with a larger BOLD response associated with longer RTs, suggesting that the IPS plays a pivotal role in intention by translating encoded information into action through evidence accumulation. Our data help to specify the functional division of labor between the IPS and TPJ and to further dissociate process components in visual search.     

Dissociable neural mechanisms for encoding predictable and unpredictable events

Attention is a necessary condition for the formation of new episodic memories, yet little is known about how dissociable attentional mechanisms for "top-down" and "bottom-up" orienting contribute to encoding. Here, subjects performed an intentional encoding task in which to-be-learned items were interspersed with irrelevant stimuli such that subjects could anticipate the appearance of some study items but not others. Subjects were more likely to later remember stimuli whose appearance was predictable at encoding. Electroencephalographic data were acquired during the study phase of the experiment to assess how synchronous neural activity related to later memory for predictable stimuli (to which attention could be oriented in a top-down fashion) and unpredictable stimuli (which rely to a greater extent on bottom-up attentional orienting). Over left frontal regions, gamma-band activity (25-55 Hz) early (approximately 150 msec) in the epoch was a robust predictor of later memory for predictable items, consistent with an emerging view that links high-frequency neural synchrony to top-down attention. By contrast, later (approximately 400 msec) theta-band activity (4-8 Hz) over the left and midline frontal cortex predicted subsequent memory for unpredictable items, suggesting a role in bottom-up attentional orienting. These results reveal for the first time the contribution of dissociable attentional mechanisms to successful encoding and contribute to a growing literature dedicated to understanding the role of neural synchrony in cognition.     

Multi‐target attention and visual short‐term memory capacity are closely linked in the intraparietal sulcus

The existing literature suggests a critical role for both the right intraparietal sulcus (IPS) and the right temporo‐parietal junction (TPJ) in our ability to attend to multiple simultaneously‐presented lateralized targets (multi‐target attention), and the failure of this ability in extinction patients. Currently, however, the precise role of each of these areas in multi‐target attention is unclear. In this study, we combined the theory of visual attention (TVA) with functional magnetic resonance imaging (fMRI) guided continuous theta burst stimulation (cTBS) in neurologically healthy subjects to directly investigate the role of the right IPS and TPJ in multi‐target attention. Our results show that cTBS at an area of the right IPS associated with multi‐target attention elicits a reduction of visual short‐term memory capacity. This suggests that the right IPS is associated with a general capacity‐limited encoding mechanism that is engaged regardless of whether targets have to be attended or remembered. Curiously, however, cTBS to the right IPS failed to elicit extinction‐like behavior in our study, supporting previous suggestions that different areas of the right IPS may provide different contributions to multi‐target attention. CTBS to the right TPJ failed to induce a change in either TVA parameters or extinction‐like behavior.     

Probing top-down information in neocortical layer 1

Accurate perception of the environment is a constructive process that requires integration of external bottom-up sensory signals with internally generated top-down information. Decades of work have elucidated how sensory neocortex processes physical stimulus features. By contrast, examining how top-down information is encoded and integrated with bottom-up signals has been challenging using traditional neuroscience methods. Recent technological advances in functional imaging of brain-wide afferents in behaving mice have enabled the direct measurement of top-down information. Here, we review the emerging literature on encoding of these internally generated signals by different projection systems enriched in neocortical layer 1 during defined brain functions, including memory, attention, and predictive coding. Moreover, we identify gaps in current knowledge and highlight future directions for this rapidly advancing field.     

Activity and effective connectivity of parietal and occipital cortical regions during haptic shape perception

It is now widely accepted that visual cortical areas are active during normal tactile perception, but the underlying mechanisms are still not clear. The goal of the present study was to use functional magnetic resonance imaging (fMRI) to investigate the activity and effective connectivity of parietal and occipital cortical areas during haptic shape perception, with a view to potentially clarifying the role of top-down and bottom-up inputs into visual areas. Subjects underwent fMRI scanning while engaging in discrimination of haptic shape or texture, and in separate runs, visual shape or texture. Accuracy did not differ significantly between tasks. Haptic shape-selective regions, identified on a contrast between the haptic shape and texture conditions in individual subjects, were found bilaterally in the postcentral sulcus (PCS), multiple parts of the intraparietal sulcus (IPS) and the lateral occipital complex (LOC). The IPS and LOC foci tended to be shape-selective in the visual modality as well. Structural equation modelling was used to study the effective connectivity among the haptic shape-selective regions in the left hemisphere, contralateral to the stimulated hand. All possible models were tested for their fit to the correlations among the observed time-courses of activity. Two equivalent models emerged as the winners. These models, which were quite similar, were characterized by both bottom-up paths from the PCS to parts of the IPS, and top-down paths from the LOC and parts of the IPS to the PCS. We conclude that interactions between unisensory and multisensory cortical areas involve bidirectional information flow.     

Coding space within but not between objects: evidence from Balint's syndrome

The ability to make spatial judgements was examined in a patient demonstrating poor perception of multiple objects following bilateral parietal lesions, under conditions in which the presence of the stimuli to which judgements were made could be detected. The tasks required judgements of spatial length or the position of coloured parts of stimuli. We manipulated the degree to which two uprights in a display could be encoded into a single perceptual object using either stored knowledge or bottom-up cues based on 2D or 3D image relations. Performance was dependent on the presence of both bottom-up grouping and familiarity. However, connectedness in the image was not sufficient to benefit performance, when stimuli were separate objects in 3D space. This deficit in spatial judgements, arising following detection of the relevant stimulus elements, is attributed to an impairment in coding the spatial relations between separate perceptual objects. This deficit could be overcome if stimuli could be grouped in 3D, using bottom-up cues and top-down knowledge.     

The relationship between level of processing and hippocampal–cortical functional connectivity during episodic memory formation in humans

New episodic memory traces represent a record of the ongoing neocortical processing engaged during memory formation (encoding). Thus, during encoding, deep (semantic) processing typically establishes more distinctive and retrievable memory traces than does shallow (perceptual) processing, as assessed by later episodic memory tests. By contrast, the hippocampus appears to play a processing‐independent role in encoding, because hippocampal lesions impair encoding regardless of level of processing. Here, we clarified the neural relationship between processing and encoding by examining hippocampal–cortical connectivity during deep and shallow encoding. Participants studied words during functional magnetic resonance imaging and freely recalled these words after distraction. Deep study processing led to better recall than shallow study processing. For both levels of processing, successful encoding elicited activations of bilateral hippocampus and left prefrontal cortex, and increased functional connectivity between left hippocampus and bilateral medial prefrontal, cingulate and extrastriate cortices. Successful encoding during deep processing was additionally associated with increased functional connectivity between left hippocampus and bilateral ventrolateral prefrontal cortex and right temporoparietal junction. In the shallow encoding condition, on the other hand, pronounced functional connectivity increases were observed between the right hippocampus and the frontoparietal attention network activated during shallow study processing. Our results further specify how the hippocampus coordinates recording of ongoing neocortical activity into long‐term memory, and begin to provide a neural explanation for the typical advantage of deep over shallow study processing for later episodic memory. Hum Brain Mapp, 2013. © 2011 Wiley Periodicals, Inc.     

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.     

Functional connectivity with the hippocampus during successful memory formation

Although it is well established that the hippocampus is critical for episodic memory, little is known about how the hippocampus interacts with cortical regions during successful memory formation. Here, we used event-related functional magnetic resonance imaging (fMRI) to identify areas that exhibited differential functional connectivity with the hippocampus during processing of novel objects that were subsequently remembered or forgotten on a postscan test. Functional connectivity with the hippocampus was enhanced during successful, as compared with unsuccessful, memory formation, in a distributed network of limbic cortical areas-including perirhinal, orbitofrontal, and retrosplenial/posterior cingulate cortex-that are anatomically connected with the hippocampal formation. Increased connectivity was also observed in lateral temporal, medial parietal, and medial occipital cortex. These findings demonstrate that successful memory formation is associated with transient increases in cortico-hippocampal interaction.     

Orienting attention in time activates left intraparietal sulcus for both perceptual and motor task goals

Attention can be directed not only toward a location in space but also to a moment in time ("temporal orienting"). Temporally informative cues allow subjects to predict when an imminent event will occur, thereby speeding responses to that event. In contrast to spatial orienting, temporal orienting preferentially activates left inferior parietal cortex. Yet, left parietal cortex is also implicated in selective motor attention, suggesting its activation during temporal orienting could merely reflect incidental engagement of preparatory motor processes. Using fMRI, we therefore examined whether temporal orienting would still activate left parietal cortex when the cued target required a difficult perceptual discrimination rather than a speeded motor response. Behaviorally, temporal orienting improved accuracy of target identification as well as speed of target detection, demonstrating the general utility of temporal cues. Crucially, temporal orienting selectively activated left inferior parietal cortex for both motor and perceptual versions of the task. Moreover, conjunction analysis formally revealed a region deep in left intraparietal sulcus (IPS) as common to both tasks, thereby identifying it as a core neural substrate for temporal orienting. Despite the context-independent nature of left IPS activation, complementary psychophysiological interaction analysis revealed how the functional connectivity of left IPS changed as a function of task context. Specifically, left IPS activity covaried with premotor activity during motor temporal orienting but with visual extrastriate activity during perceptual temporal orienting, thereby revealing a cooperative network that comprises both temporal orienting and task-specific processing nodes.     

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.     

Appearing and disappearing stimuli trigger a reflexive modulation of visual cortical activity

From the vast array of stimuli continually inundating our senses, only a very small portion is selected for higher-order processing. This selection is influenced by voluntary and reflexive mechanisms that may act at multiple stages of analysis. Extensive research has revealed that top-down voluntary mechanisms modulate information processing at both "early" (e.g., perceptual) and "late" (e.g., semantic) stages. Bottom-up sensory-driven mechanisms, however, are less well understood. Previous investigations of bottom-up mechanisms may have been influenced by top-down mechanisms because the stimuli were task-relevant and required overt responses. Here, we directly measured bottom-up influences on visual information processing by recording event-related brain potentials (ERP) to sequences of task-irrelevant visual stimuli. We found that abrupt visual events triggered an automatic enhancement of extrastriate visual activity (the P1 ERP component) to subsequent visual stimuli occurring at the same location. In contrast to theories suggesting that the abrupt appearance of a new object is unique in being able to trigger bottom-up effects, we found that disappearing objects triggered the same enhancement of subsequent stimulus processing as did appearing objects. The present data, however, also provide new electrophysiological evidence for a level of analysis in the brain that may be specific to the appearance of new objects. These data thus provide evidence that abruptly appearing objects may evoke specialized processing at certain stages of analysis in the brain but that, despite this difference, appearing and disappearing objects both trigger reflexive mechanisms that bias neural activity in human extrastriate visual cortex.     

Hippocampal control of repetition effects for associative stimuli

Recent findings suggest that repetition effects interact with episodic memory processes that are putatively supported by the hippocampus. Thus, the formation or refinement of episodic memories may be related to a modulating signal from the hippocampus to the neocortex which leads to sparser or more extended stimulus representations (repetition suppression or enhancement), depending on the type of stimulus and the brain site. This framework suggests that hippocampal activity during the initial presentation of a stimulus correlates with the magnitude of repetition effects. Here, we tested this hypothesis in an fMRI study in which associations between faces and buildings were presented twice. BOLD responses showed repetition suppression in fusiform face area (FFA) and parahippocampal place area (PPA), most likely due to a refinement of existing category representations. Hippocampal activity during the first presentations was correlated with the amount of repetition suppression, in particular in the FFA. Repetition enhancement effects were observed on BOLD responses in posterior parietal cortex, possibly related to the formation of new representations of associative stimuli. The magnitude of parietal BOLD repetition effects depended on successful memory formation. These findings suggest that both repetition enhancement and repetition suppression effects are influenced by a modulating signal from the hippocampus. © 2014 Wiley Periodicals, Inc.     

Multi-voxel patterns of visual category representation during episodic encoding are predictive of subsequent memory

Successful encoding of episodic memories is thought to depend on contributions from prefrontal and temporal lobe structures. Neural processes that contribute to successful encoding have been extensively explored through univariate analyses of neuroimaging data that compare mean activity levels elicited during the encoding of events that are subsequently remembered vs. those subsequently forgotten. Here, we applied pattern classification to fMRI data to assess the degree to which distributed patterns of activity within prefrontal and temporal lobe structures elicited during the encoding of word-image pairs were diagnostic of the visual category (Face or Scene) of the encoded image. We then assessed whether representation of category information was predictive of subsequent memory. Classification analyses indicated that temporal lobe structures contained information robustly diagnostic of visual category. Information in prefrontal cortex was less diagnostic of visual category, but was nonetheless associated with highly reliable classifier-based evidence for category representation. Critically, trials associated with greater classifier-based estimates of category representation in temporal and prefrontal regions were associated with a higher probability of subsequent remembering. Finally, consideration of trial-by-trial variance in classifier-based measures of category representation revealed positive correlations between prefrontal and temporal lobe representations, with the strength of these correlations varying as a function of the category of image being encoded. Together, these results indicate that multi-voxel representations of encoded information can provide unique insights into how visual experiences are transformed into episodic memories.     

Episodic memory: Neuronal codes for what,where, and when

Episodic memory is defined as the ability to recall events in a spatiotemporal context. Formation of such memories is critically dependent on the hippocampal formation and its inputs from the entorhinal cortex. To be able to support the formation of episodic memories, entorhinal cortex and hippocampal formation should contain a neuronal code that follows several requirements. First, the code should include information about position of the agent (“where”), sequence of events (“when”), and the content of the experience itself (“what”). Second, the code should arise instantly thereby being able to support memory formation of one‐shot experiences. For successful encoding and to avoid interference between memories during recall, variations in location, time, or in content of experience should result in unique ensemble activity. Finally, the code should capture several different resolutions of experience so that the necessary details relevant for future memory‐based predictions will be stored. We review how neuronal codes in entorhinal cortex and hippocampus follow these requirements and argue that during formation of episodic memories entorhinal cortex provides hippocampus with instant information about ongoing experience. Such information originates from (a) spatially modulated neurons in medial entorhinal cortex, including grid cells, which provide a stable and universal positional metric of the environment; (b) a continuously varying signal in lateral entorhinal cortex providing a code for the temporal progression of events; and (c) entorhinal neurons coding the content of experiences exemplified by object‐coding and odor‐selective neurons. During formation of episodic memories, information from these systems are thought to be encoded as unique sequential ensemble activity in hippocampus, thereby encoding associations between the content of an event and its spatial and temporal contexts. Upon exposure to parts of the encoded stimuli, activity in these ensembles can be reinstated, leading to reactivation of the encoded activity pattern and memory recollection.     

Aspects of psychodynamic neuropsychiatry I: episodic memory, transference, and the oddball paradigm

Psychotherapy has, since the time of Freud, focused on the unconscious and dynamically repressed memory. This article explores a therapy where the focus is on what is known, on episodic memory. Episodic memory, along with semantic memory, is part of the declarative memory system. Episodic memory depends on frontal, parietal, as well as temporal lobe function. It is the system related to the encoding and recall of context-rich memory. While memory usually decays with time, powerfully encoded episodic memory may augment. This article explores the hypothesis that such augmentation is the result of conditioning and kindling. Augmented memory could lead to a powerful "top-down" focus of attention-such that one would perceive only what one had set out to perceive. The "oddball paradigm" is suggested as a route out of such a self-perpetuating system. A clinical example (a disguised composite of several clinical histories) is used to demonstrate how such an intensification of memory and attention came about as a result of the transference, and how the "oddball paradigm" was used as a way out of what had become a treatment stalemate.