Melina R. Uncapher

Posterior parietal cortex and episodic encoding: insights from fMRI subsequent memory effects and dual-attention theory.

The formation of episodic memories--memories for life events--is affected by attention during event processing. A leading neurobiological model of attention posits two separate yet interacting systems that depend on distinct regions in lateral posterior parietal cortex (PPC). From this dual-attention perspective, dorsal PPC is thought to support the goal-directed allocation of attention, whereas ventral PPC is thought to support reflexive orienting to information that automatically captures attention. To advance understanding of how parietal mechanisms may impact event encoding, we review functional MRI studies that document the relationship between lateral PPC activation during encoding and subsequent memory performance (e.g., later remembering or forgetting). This review reveals that (a) encoding-related activity is frequently observed in human lateral PPC, (b) increased activation in dorsal PPC is associated with later memory success, and (c) increased activation in ventral PPC predominantly correlates with later memory failure. From a dual-attention perspective, these findings suggest that allocating goal-directed attention during event processing increases the probability that the event will be remembered later, whereas the capture of reflexive attention during event processing may have negative consequences for event encoding. The prevalence of encoding-related activation in parietal cortex suggests that neurobiological models of episodic memory should consider how parietal-mediated attentional mechanisms regulate encoding.

Posterior parietal cortex and episodic retrieval: Convergent and divergent effects of attention and memory

Functional neuroimaging studies of humans engaged in retrieval from episodic memory have revealed a surprisingly consistent pattern of retrieval-related activity in lateral posterior parietal cortex (PPC). Given the well-established role of lateral PPC in subserving goal-directed and reflexive attention, it has been hypothesized that PPC activation during retrieval reflects the recruitment of parietal attention mechanisms during remembering. Here, we evaluate this hypothesis by considering the anatomical overlap of retrieval and attention effects in lateral PPC. We begin by briefly reviewing the literature implicating dorsal PPC in goal-directed attention and ventral PPC in reflexive attention. We then discuss the pattern of dorsal and ventral PPC activation during episodic retrieval, and conclude with consideration of the degree of anatomical convergence across the two domains. This assessment revealed that predominantly divergent subregions of lateral PPC are engaged during acts of episodic retrieval and during goal-directed and reflexive attention, suggesting that PPC retrieval effects reflect functionally distinct mechanisms from these forms of attention. Although attention must play a role in aspects of retrieval, the data reviewed here suggest that further investigation into the relationship between processes of attention and memory, as well as alternative accounts of PPC contributions to retrieval, is warranted.

Episodic Encoding Is More than the Sum of Its Parts: An fMRI Investigation of Multifeatural Contextual Encoding

Episodic memories are characterized by their contextual richness, yet little is known about how the various features comprising an episode are brought together in memory. Here we employed fMRI and a multidimensional source memory procedure to investigate processes supporting the mnemonic binding of item and contextual information. Volunteers were scanned while encoding items for which the contextual features (color and location) varied independently, allowing activity elicited at the time of study to be segregated according to whether both, one, or neither feature was successfully retrieved on a later memory test. Activity uniquely associated with successful encoding of both features was identified in the intra-parietal sulcus, a region strongly implicated in the support of attentionally mediated perceptual binding. The findings suggest that the encoding of disparate features of an episode into a common memory representation requires that the features be conjoined in a common perceptual representation when the episode is initially experienced.

Content-specificity of the neural correlates of recollection.

It is widely assumed that episodic retrieval (recollection) involves reinstatement of cortical activity engaged during the processing of an episode when it was initially experienced. It follows from this assumption that the cortical correlates of recollection should differ with the content of what is recollected, and that retrieval of different content should be associated with activity in functionally distinct cortical regions. The present experiment investigated these predictions. Subjects (N=17) studied a mixed list of words and pictures and were then presented with a test list comprised of words only. Test items were studied words, the names of studied pictures, and unstudied (new) words. Functional magnetic resonance images were acquired while the subjects made Remember/Know/New judgments to these test words. Independent of study material, studied items endorsed as Remembered elicited greater activity than correctly classified unstudied items in several regions, including left frontal, left lateral parietal, and posterior cingulate cortex. In addition, Remembered items elicited greater activity in the right hippocampus and parahippocampal gyrus than items accorded Know judgments, replicating previous findings. Analysis of content-specific effects demonstrated a regional double-dissociation within left fusiform cortex; recollected words elicited greater activity than recollected pictures in lateral fusiform, whereas the reverse effect was evident in an anterior fusiform region. The lateral and anterior fusiform areas correspond closely to areas held to be functionally specialized for the processing of visual words and pictures, respectively. Thus, the current findings support the cortical reinstatement hypothesis of episodic retrieval.

Chapter 21 Encoding-retrieval overlap in human episodic memory: A functional neuroimaging perspective

The principle of transfer-appropriate processing and the cortical reinstatement hypothesis are two influential theoretical frameworks, articulated at the psychological and neurobiological levels of explanation, respectively, that each propose that the processes supporting the encoding and retrieval of episodic information are strongly interdependent. Here, we integrate these two frameworks into a single model that generates predictions that can be tested using functional neuroimaging methods in healthy humans, and then go on to describe findings that are in accord with these predictions. Consistent with the transfer-appropriate processing and cortical reinstatement frameworks, the neural correlates of successful encoding vary according to how retrieval is cued, and the neural correlates of retrieval are modulated by how items are encoded. Thus, encoding and retrieval should not be viewed as separate stages of memory that can be investigated in isolation from one another.

Functional Heterogeneity in Posterior Parietal Cortex Across Attention and Episodic Memory Retrieval

While attention is critical for event memory, debate has arisen regarding the extent to which posterior parietal cortex (PPC) activation during episodic retrieval reflects engagement of PPC-mediated mechanisms of attention. Here, we directly examined the relationship between attention and memory, within and across subjects, using functional magnetic resonance imaging attention-mapping and episodic retrieval paradigms. During retrieval, 4 functionally dissociable PPC regions were identified. Specifically, 2 PPC regions positively tracked retrieval outcomes: lateral intraparietal sulcus (latIPS) indexed graded item memory strength, whereas angular gyrus (AnG) tracked recollection. By contrast, 2 other PPC regions demonstrated nonmonotonic relationships with retrieval: superior parietal lobule (SPL) tracked retrieval reaction time, consistent with a graded engagement of top-down attention, whereas temporoparietal junction displayed a complex pattern of below-baseline retrieval activity, perhaps reflecting disengagement of bottom-up attention. Analyses of retrieval effects in PPC topographic spatial attention maps (IPS0-IPS5; SPL1) revealed that IPS5 and SPL1 exhibited a nonmonotonic relationship with retrieval outcomes resembling that in the SPL region, further suggesting that SPL activation during retrieval reflects top-down attention. While demands on PPC attention mechanisms vary during retrieval attempts, the present functional parcellation of PPC indicates that 2 additional mechanisms (mediated by latIPS and AnG) positively track retrieval outcomes.

Encoding and the Durability of Episodic Memory: A Functional Magnetic Resonance Imaging Study

Memories vary in their durability even when encoding conditions apparently remain constant. We investigated whether, under these circumstances, memory durability is nonetheless associated with variation in the neural activity elicited during encoding. Event-related functional magnetic resonance imaging data were acquired while volunteers semantically classified visually presented words. Using the “remember/know” procedure, memory for one-half of the words was tested after 30 min and for the remaining half after 48 h. In several regions, including left hippocampus and left dorsal inferior frontal gyrus (IFG), activity at encoding differed depending on whether items were later recollected regardless of study-test delay. Delay-selective effects were also evident, however. Recollection after 48 h was associated with enhanced activity in bilateral ventral IFG, whereas recollection after 30 min was associated with greater fusiform activity. Thus, there is a relationship between the neural activity elicited by an event as it is encoded and the durability of the resulting memory representation.

Selecting for memory? The influence of selective attention on the mnemonic binding of contextual information

Not all of what is experienced is remembered later. Behavioral evidence suggests that the manner in which an event is processed influences which aspects of the event will later be remembered. The present experiment investigated the neural correlates of “selective encoding,” or the mechanisms that support the encoding of some elements of an event in preference to others. Event-related MRI data were acquired while volunteers selectively attended to one of two different contextual features of study items (color or location). A surprise memory test for the items and both contextual features was subsequently administered to determine the influence of selective attention on the neural correlates of contextual encoding. Activity in several cortical regions indexed later memory success selectively for color or location information, and this encoding-related activity was enhanced by selective attention to the relevant feature. Critically, a region in the hippocampus responded selectively to attended source information (whether color or location), demonstrating encoding-related activity for attended but not for nonattended source features. Together, the findings suggest that selective attention modulates the magnitude of activity in cortical regions engaged by different aspects of an event, and hippocampal encoding mechanisms seem to be sensitive to this modulation. Thus, the information that is encoded into a memory representation is biased by selective attention, and this bias is mediated by cortical–hippocampal interactions.

Dissociable Effects of Top-Down and Bottom-Up Attention during Episodic Encoding

It is well established that the formation of memories for lifes 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.

Effects of Divided Attention on fMRI Correlates of Memory Encoding

Performing a secondary task concurrently with a study task has a detrimental effect on later memory for studied items. To investigate the mechanisms underlying this effect, the processing resources available for an incidental encoding task were varied by manipulating secondary task difficulty. fMRI data were acquired as volunteers (n = 16) made animacy decisions to visually presented study words while concurrently performing either an easy or a hard auditory monitoring task. Subsequent memory effects-greater activity at study for words later remembered versus words later forgotten-were identified in the left ventral inferior frontal gyrus and the left anterior hippocampus. These effects did not vary according to whether the encoding task was performed concurrently with the easy or the hard secondary task. However, as secondary task difficulty increased, study-item activity declined and auditory-item activity increased in dorsolateral prefrontal and superior parietal regions that have been implicated in the support of executive and control functions. The findings suggest that dividing attention during encoding influences the probability of engaging the encoding operations that support later episodic memory, but does not alter the nature of the operations themselves. The findings further suggest that the probability of engaging these encoding operations depends on the level of general processing resources engaged in service of the study task.