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Ranganath, C.

Publications and source records attributed to Ranganath, C..

32 records · Page 2Linked to original sources

A cortico-hippocampal scaffold for representing and recalling lifelike events

Although every life event is unique, there are considerable commonalities across events. However, little is known about whether or how the brain flexibly represents information about different event components at encoding and during remembering. Here, we show that different cortico-hippocampal networks systematically represent specific components of events depicted in videos, both during viewing and during episodic memory retrieval. Regions of an Anterior Temporal Network represented information about people, generalizing across contexts, whereas regions of a Posterior Medial Network represented context information, generalizing across people. Medial prefrontal cortex generalized across videos depicting the same schema, whereas the hippocampus maintained event-specific representations. Similar effects were seen in real-time and recall, suggesting reuse of event components across overlapping episodic memories. These findings reveal a computationally optimal strategy in cortico-hippocampal networks for encoding different high-level event components, supporting efficient reuse for event comprehension, imagination, and recollection.

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Bridges, not walls: the hippocampus builds narrative memories across distant events

Lifes events are scattered throughout time, yet we often recall different events in the context of an integrated narrative. Prior research suggests that the hippocampus, which supports memory for past events, can sometimes support integration of overlapping associations or separate events, but the conditions which lead to hippocampus-dependent memory integration are unclear. We used functional brain imaging to test whether the ability to form a larger narrative (narrative coherence) drives hippocampal memory integration. During encoding of fictional stories, the hippocampus supported patterns of activity, including activity at boundaries between events, which were more similar between distant events that formed one coherent narrative, compared with events taken from unrelated narratives. Twenty-four hours later, the hippocampus preferentially supported detailed recall of coherent narrative events, through reinstatement of hippocampal activity patterns from encoding. These findings reveal a key function of the hippocampus: the dynamic integration of events into a narrative structure for memory.

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Organization of cortico-hippocampal networks in the human brain

Episodic memory depends on interactions between the hippocampus and the interconnected regions comprising default mode network (DMN). Here, using data-driven analyses of resting-state fMRI data, we identified the networks that interact with the hippocampus--the DMN and a "Medial Temporal Network" (MTN) that included regions in the medial temporal lobe and retrosplenial cortex. We observed that the MTN plays a critical role in connecting the visual network to the DMN and hippocampus. The DMN could be further divided into three subnetworks: a "Posterior-Medial" Subnetwork comprised of posterior cingulate, and lateral parietal cortices, an "Anterior-Temporal" Subnetwork comprised of regions in the temporopolar, and dorsomedial prefrontal cortex, and a "Medial-Prefrontal" Subnetwork comprised of regions primarily in the medial prefrontal cortex. These networks vary in their functional connectivity along the hippocampal long-axis and represent different kinds of information during memory-guided decision-making. Finally, a Neurosynth meta-analysis of fMRI studies suggests new hypotheses regarding the functions of the MTN and DMN subnetworks, providing a framework to guide future research on the neural architecture of episodic memory.

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Map making: Constructing, combining, and navigating abstract cognitive maps

Cognitive maps are thought to enable model-based inferences from limited experience that can guide novel decisions-a hallmark of behavioral flexibility. We tested whether the hippocampus (HC), entorhinal cortex (EC), and ventromedial prefrontal cortex (vmPFC)/medial orbitofrontal cortex (mOFC) organize abstract and discrete relational information into a cognitive map to guide novel inferences. Subjects learned the status of people in two separate unseen 2-D social hierarchies defined by competence and popularity piecemeal from binary comparisons, with each dimension learned on a separate day. Although only one dimension was ever behaviorally relevant, multivariate activity patterns in HC, EC and vmPFC/mOFC were linearly related to the Euclidean distance between people in the mentally reconstructed 2-D space. Hubs created unique comparisons between the two hierarchies, enabling inferences between novel pairs of people. We found that both behavior and neural activity in EC and vmPFC/mOFC reflected the Euclidean distance to the retrieved hub, which was reinstated in HC. These findings reveal how abstract and discrete relational structures are represented, combined, and enable novel inferences in the human brain.

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Representation of Task Structure in Human Hippocampus

The hippocampus is thought to support episodic memory, or memory for specific events, but recent work also suggests that it may be involved in extracting structure from the world to guide future decisions and predictions. Recent evidence in rodents suggests that the hippocampus supports decision-making in cooperation with orbitofrontal cortex (OFC), possibly based on representation of task structure. Here, we used functional magnetic resonance imaging (fMRI) to test how the human hippocampus and OFC represents decision-relevant information extracted from previous experiences. Participants performed a task in which they learned values of different foods in grocery store contexts. The task was structured such that we could examine the degree to which neural representations could reflect generalized information about different task structures. Specifically, we manipulated whether a foods desirability varied with store context or not. Some foods were desirable in some store contexts and not in others; some foods were always desirable or undesirable. Participants needed to extract these two task sub-structures (i.e., context-determined vs. context-invariant) from the task structure. We examined hippocampal and OFC activity patterns during a decision-making task after participants were trained with the task structure. Our results showed that both hippocampus and OFC carried task structure information that was relevant to the decision outcomes. Hippocampal and lateral OFC representations differentiated between context-determined (deterministic) and context-invariant (probabilistic) task structures. The degree of this differentiation, an index of task structure representation, was highly correlated between hippocampus and lateral OFC. These results add to a mounting evidence suggesting that the hippocampus and OFC support decision-making by representing task relevant information to the decision outcomes after the task structure is learned.

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Structured event memory: a neuro-symbolic model of event cognition

Humans spontaneously organize a continuous experience into discrete events and use the learned structure of these events to generalize and organize memory. We introduce the Structured Event Memory (SEM) model of event cognition, which accounts for human abilities in event segmentation, memory, and generalization. SEM is derived from a probabilistic generative model of event dynamics defined over structured symbolic scenes. By embedding symbolic scene representations in a vector space and parametrizing the scene dynamics in this continuous space, SEM combines the advantages of structured and neural network approaches to high-level cognition. Using probabilistic reasoning over this generative model, SEM can infer event boundaries, learn event schemata, and use event knowledge to reconstruct past experience. We show that SEM can scale up to high-dimensional input spaces, producing human-like event segmentation for naturalistic video data, and accounts for a wide array of memory phenomena.

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Dynamic integration of conceptual information during learning

The development and application of concepts is a critical component of cognition. Although concepts can be formed on the basis of simple perceptual or semantic features, conceptual representations can also capitalize on similarities across feature relationships. By representing these types of higher-order relationships, concepts can simplify the learning problem and facilitate decisions. Despite this, little is known about the neural mechanisms that support the construction and deployment of these kinds of higher-order concepts during learning. To address this question, we combined a carefully designed associative learning task with computational model-based functional magnetic resonance imaging (fMRI). Participants were scanned as they learned and made decisions about sixteen pairs of cues and associated outcomes. Associations were structured such that individual cues shared feature relationships, operationalized as shared patterns of cue pair-outcome associations. In order to capture the large number of possible conceptual representational structures that participants might employ and to evaluate how conceptual representations are used during learning, we leveraged a well-specified Bayesian computational model of category learning [1]. Behavioral and model-based results revealed that participants who displayed a tendency to link experiences in memory benefitted from faster learning rates, suggesting that the use of the conceptual structure in the task facilitated decisions about cue pair-outcome associations. Model-based fMRI analyses revealed that trial-by-trial integration of cue information into higher-order conceptual representations was supported by an anterior temporal (AT) network of regions previously implicated in representing complex conjunctions of features and meaning-based information.

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Dissociable medial temporal pathways for encoding emotional item and context information

Emotional experiences are typically remembered with a greater sense of recollection than neutral experiences, but memory benefits for emotional items do not typically extend to their source contexts. Item and source memory have been attributed to different subregions of the medial temporal lobes (MTL), but it is unclear how emotional item recollection fits into existing models of MTL function and, in particular, what is the role of the hippocampus. To address these issues, we used high-resolution functional magnetic resonance imaging (fMRI) to examine MTL contributions to successful emotional item and context encoding. The results showed that emotional items were recollected more often than neutral items. Whereas amygdala and perirhinal cortex (PRC) activity supported the recollection advantage for emotional items, hippocampal and parahippocampal cortex activity predicted subsequent source memory for both types of items, reflecting a double dissociation between anterior and posterior MTL regions. In addition, amygdala activity during encoding modulated the relationships of PRC activity and hippocampal activity to subsequent item recollection and source memory, respectively. Specifically, whereas PRC activity best predicted subsequent item recollection when amygdala activity was relatively low, hippocampal activity best predicted source memory when amygdala activity was relatively high. We interpret these findings in terms of complementary compared to synergistic amygdala-MTL interactions. The results suggest that emotion-related enhancements in item recollection are supported by an amygdala-PRC pathway, which is separable from the hippocampal pathway that binds items to their source context.

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Neural oscillations during conditional associative learning

Associative learning requires mapping between complex stimuli and behavioural responses. When multiple stimuli are involved, conditional associative learning is a gradual process with learning based on trial and error. It is established that a distributed network of regions track associative learning, however the role of neural oscillations in human learning remains less clear. Here we used scalp EEG to test how neural oscillations change during learning of arbitrary visuo-motor associations. Participants learned to associative 48 different abstract shapes to one of four button responses through trial and error over repetitions of the shapes. To quantify how well the associations were learned for each trial, we used a state-space computational model of learning that provided a probability of each trial being correct given past performance for that stimulus, that we take as a measure of the strength of the association. We used linear modelling to relate single-trial neural oscillations to single-trial measures of association strength. We found frontal midline theta oscillations during the delay period tracked learning, where theta activity was strongest during the early stages of learning and declined as the associations were formed. Further, posterior alpha and low-beta oscillations in the cue period showed strong desynchronised activity early in learning, while stronger alpha activity during the delay period were seen as associations became well learned. Moreover, the magnitude of these effects during early learning, before the associations were learned, related to improvements in memory seen on the next presentation of the stimulus. The current study provides clear evidence that frontal theta and posterior alpha/beta oscillations play a key role during associative memory formation.

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Time Regained: How the Human Brain Constructs Memory for Time

Lifes episodes unfold against a context that changes with time. Recent neuroimaging studies have revealed significant findings about how specific areas of the human brain may support the representation of temporal information in memory. A consistent theme in these studies is that the hippocampus appears to play a central role in representing temporal context, as operationalized in neuroimaging studies of arbitrary lists of items, sequences of items, or meaningful, lifelike events. Additionally, activity in a posterior medial cortical network may reflect the representation of generalized temporal information for meaningful events. The hippocampus, posterior medial network, and other regions--particularly in prefrontal cortex--appear to play complementary roles in memory for temporal context.\n\nHighlightsO_LIThe hippocampus encodes information about temporal contiguity, order, and event structure.\nC_LIO_LIPosterior medial cortical areas represent order across meaningfully coherent events.\nC_LIO_LIPrefrontal and subcortical contributions to temporal memory deserve further study.\nC_LI

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Space, Time and Episodic Memory: the Hippocampus is all over the Cognitive Map

In recent years, the field has reached an impasse between models suggesting that the hippocampus is fundamentally involved in spatial processing and models suggesting that the hippocampus automatically encodes all dimensions of experience in the service of memory. Here, we consider key conceptual issues that have impeded progress in our understanding of hippocampal function, and we review findings that establish the scope and limits of hippocampal involvement in navigation and memory. We argue that space and time serve as a primary scaffold to break up experiences into specific contexts, and to organize multimodal input that is to be associated within a context. However, the hippocampus is clearly capable of incorporating additional dimensions into the scaffold if they are determined to be relevant in the event-defined context. Conceiving of the hippocampal representation as constrained by immediate task demands--yet preferring axes that involve space and time--helps to reconcile an otherwise disparate set of findings on the core function of the hippocampus.

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Theta Phase Synchronization Between The Human Hippocampus And The Prefrontal Cortex Supports Learning Of Unexpected Information

Events that violate predictions are thought to not only modulate activity within the hippocampus and prefrontal cortex, but also to enhance communication between the two regions. Several studies in rodents have shown that synchronized theta oscillations facilitate communication between the prefrontal cortex and hippocampus during salient events, but it remains unclear whether similar oscillatory mechanisms support interactions between the two regions in humans. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and prefrontal cortex from two patients undergoing presurgical evaluation for pharmaco-resistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal-prefrontal theta phase synchronization was significantly higher during encoding of unexpected study items, compared to contextually expected study items. In contrast, we did not find increased theta synchronization between the prefrontal cortex and rhinal cortex. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and prefrontal cortex during the processing of contextually salient information.

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CA1 And CA3 Differentially Support Spontaneous Retrieval Of Episodic Contexts Within Human Hippocampal Subfields

The hippocampus plays a critical role in spatial and episodic memory. Mechanistic models predict that hippocampal subfields have computational specializations that differentially support memory. However, there is little empirical evidence suggesting differences between the subfields, particularly in humans. To clarify how hippocampal subfields support human spatial and episodic memory, we developed a virtual reality paradigm where participants passively navigated through houses (spatial contexts) across a series of videos (episodic contexts). We then used multivariate analyses of high-resolution fMRI data to identify neural representations of contextual information during recollection. Multi-voxel pattern similarity analyses revealed that CA1 represented objects that shared an episodic context as more similar than those from different episodic contexts. CA23DG showed the opposite pattern, differentiating between objects encountered in the same episodic context. The complementary characteristics of these subfields explain how we can parse our experiences into cohesive episodes while retaining the specific details that support vivid recollection.

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Alpha Oscillations During Incidental Encoding Predict Subsequent Memory For New "Foil" Information

People can employ adaptive strategies to increase the likelihood that previously encoded information will be successfully retrieved. One such strategy is to constrain retrieval towards relevant information by re-implementing the neurocognitive processes that were engaged during encoding. Using electroencephalography (EEG), we examined the temporal dynamics with which constraining retrieval towards semantic versus non-semantic information affects the processing of new \"foil\" information encountered during a memory test. Time-frequency analysis of EEG data acquired during an initial study phase revealed that semantic compared to non-semantic processing was associated with alpha decreases in a left frontal electrode cluster from around 600ms after stimulus onset. Successful encoding of semantic versus non-semantic foils during a subsequent memory test was related to decreases in alpha oscillatory activity in the same left frontal electrode cluster, which emerged relatively late in the trial at around 1000-1600ms after stimulus onset. Across subjects, left frontal alpha power elicited by semantic processing during the study phase correlated significantly with left frontal alpha power associated with semantic foil encoding during the memory test. Furthermore, larger left frontal alpha power decreases elicited by semantic foil encoding during the memory test predicted better subsequent semantic foil recognition in an additional surprise foil memory test. These findings indicate that constraining retrieval towards semantic information involves re-implementing semantic encoding operations that are mediated by alpha oscillations, and that such re-implementation occurs at a late stage of memory retrieval perhaps reflecting additional monitoring processes.

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