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  1. Article: Distinct hippocampal mechanisms support concept formation and updating.

    Mack, Michael L / Love, Bradley C / Preston, Alison R

    bioRxiv : the preprint server for biology

    2024  

    Abstract: Learning systems must constantly decide whether to create new representations or update existing ones. For example, a child learning that a bat is a mammal and not a bird would be best served by creating a new representation, whereas updating may be best ...

    Abstract Learning systems must constantly decide whether to create new representations or update existing ones. For example, a child learning that a bat is a mammal and not a bird would be best served by creating a new representation, whereas updating may be best when encountering a second similar bat. Characterizing the neural dynamics that underlie these complementary memory operations requires identifying the exact moments when each operation occurs. We address this challenge by interrogating fMRI brain activation with a computational learning model that predicts trial-by-trial when memories are created versus updated. We found distinct neural engagement in anterior hippocampus and ventral striatum for model-predicted memory create and update events during early learning. Notably, the degree of this effect in hippocampus, but not ventral striatum, significantly related to learning outcome. Hippocampus additionally showed distinct patterns of functional coactivation with ventromedial prefrontal cortex and angular gyrus during memory creation and premotor cortex during memory updating. These findings suggest that complementary memory functions, as formalized in computational learning models, underlie the rapid formation of novel conceptual knowledge, with the hippocampus and its interactions with frontoparietal circuits playing a crucial role in successful learning.
    Significance statement: How do we reconcile new experiences with existing knowledge? Prominent theories suggest that novel information is either captured by creating new memories or leveraged to update existing memories, yet empirical support of how these distinct memory operations unfold during learning is limited. Here, we combine computational modeling of human learning behaviour with functional neuroimaging to identify moments of memory formation and updating and characterize their neural signatures. We find that both hippocampus and ventral striatum are distinctly engaged when memories are created versus updated; however, it is only hippocampus activation that is associated with learning outcomes. Our findings motivate a key theoretical revision that positions hippocampus is a key player in building organized memories from the earliest moments of learning.
    Language English
    Publishing date 2024-02-15
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2024.02.14.580181
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  2. Article ; Online: Memory reactivation and suppression modulate integration of the semantic features of related memories in hippocampus.

    Morton, Neal W / Zippi, Ellen L / Preston, Alison R

    Cerebral cortex (New York, N.Y. : 1991)

    2023  Volume 33, Issue 14, Page(s) 9020–9037

    Abstract: Encoding an event that overlaps with a previous experience may involve reactivating an existing memory and integrating it with new information or suppressing the existing memory to promote formation of a distinct, new representation. We used fMRI during ... ...

    Abstract Encoding an event that overlaps with a previous experience may involve reactivating an existing memory and integrating it with new information or suppressing the existing memory to promote formation of a distinct, new representation. We used fMRI during overlapping event encoding to track reactivation and suppression of individual, related memories. We further used a model of semantic knowledge based on Wikipedia to quantify both reactivation of semantic knowledge related to a previous event and formation of integrated memories containing semantic features of both events. Representational similarity analysis revealed that reactivation of semantic knowledge related to a prior event in posterior medial prefrontal cortex (pmPFC) supported memory integration during new learning. Moreover, anterior hippocampus (aHPC) formed integrated representations combining the semantic features of overlapping events. We further found evidence that aHPC integration may be modulated on a trial-by-trial basis by interactions between ventrolateral PFC and anterior mPFC, with suppression of item-specific memory representations in anterior mPFC inhibiting hippocampal integration. These results suggest that PFC-mediated control processes determine the availability of specific relevant memories during new learning, thus impacting hippocampal memory integration.
    MeSH term(s) Semantics ; Learning ; Prefrontal Cortex/diagnostic imaging ; Prefrontal Cortex/physiology ; Hippocampus/diagnostic imaging ; Hippocampus/physiology ; Magnetic Resonance Imaging ; Memory, Episodic ; Brain Mapping/methods
    Language English
    Publishing date 2023-06-05
    Publishing country United States
    Document type Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
    ZDB-ID 1077450-6
    ISSN 1460-2199 ; 1047-3211
    ISSN (online) 1460-2199
    ISSN 1047-3211
    DOI 10.1093/cercor/bhad179
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  3. Article: Concept formation as a computational cognitive process.

    Morton, Neal W / Preston, Alison R

    Current opinion in behavioral sciences

    2021  Volume 38, Page(s) 83–89

    Abstract: Hippocampus and entorhinal cortex form cognitive maps that represent relations among memories within a multidimensional space. While these relational maps have long been proposed to contribute to episodic memory, recent work suggests that they also ... ...

    Abstract Hippocampus and entorhinal cortex form cognitive maps that represent relations among memories within a multidimensional space. While these relational maps have long been proposed to contribute to episodic memory, recent work suggests that they also support concept formation by representing relevant features for discriminating among related concepts. Cognitive maps may be refined by medial prefrontal cortex, which selects dimensions to represent based on their behavioral relevance. Hippocampal pattern completion, which is critical for retrieval of episodic memories, may also contribute to generalization of existing concepts to new exemplars. Navigation within hippocampal cognitive maps, which is guided by grid coding in entorhinal cortex, may contribute to imagination through recombination of event elements or concept features.
    Language English
    Publishing date 2021-01-08
    Publishing country Netherlands
    Document type Journal Article
    ISSN 2352-1546
    ISSN 2352-1546
    DOI 10.1016/j.cobeha.2020.12.005
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  4. Article ; Online: Development of human hippocampal subfield microstructure and relation to associative inference.

    Vinci-Booher, Sophia / Schlichting, Margaret L / Preston, Alison R / Pestilli, Franco

    Cerebral cortex (New York, N.Y. : 1991)

    2023  Volume 33, Issue 18, Page(s) 10207–10220

    Abstract: The hippocampus is a complex brain structure composed of subfields that each have distinct cellular organizations. While the volume of hippocampal subfields displays age-related changes that have been associated with inference and memory functions, the ... ...

    Abstract The hippocampus is a complex brain structure composed of subfields that each have distinct cellular organizations. While the volume of hippocampal subfields displays age-related changes that have been associated with inference and memory functions, the degree to which the cellular organization within each subfield is related to these functions throughout development is not well understood. We employed an explicit model testing approach to characterize the development of tissue microstructure and its relationship to performance on 2 inference tasks, one that required memory (memory-based inference) and one that required only perceptually available information (perception-based inference). We found that each subfield had a unique relationship with age in terms of its cellular organization. While the subiculum (SUB) displayed a linear relationship with age, the dentate gyrus (DG), cornu ammonis field 1 (CA1), and cornu ammonis subfields 2 and 3 (combined; CA2/3) displayed nonlinear trajectories that interacted with sex in CA2/3. We found that the DG was related to memory-based inference performance and that the SUB was related to perception-based inference; neither relationship interacted with age. Results are consistent with the idea that cellular organization within hippocampal subfields might undergo distinct developmental trajectories that support inference and memory performance throughout development.
    MeSH term(s) Humans ; Hippocampus ; CA2 Region, Hippocampal ; CA1 Region, Hippocampal ; Magnetic Resonance Imaging/methods ; Neuropsychological Tests
    Language English
    Publishing date 2023-08-09
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 1077450-6
    ISSN 1460-2199 ; 1047-3211
    ISSN (online) 1460-2199
    ISSN 1047-3211
    DOI 10.1093/cercor/bhad276
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  5. Article ; Online: Asynchronous development of memory integration and differentiation influences temporal memory organization.

    Coughlin, Christine / Pudhiyidath, Athula / Roome, Hannah E / Varga, Nicole L / Nguyen, Kim V / Preston, Alison R

    Developmental science

    2023  Volume 27, Issue 2, Page(s) e13437

    Abstract: Adults remember items with shared contexts as occurring closer in time to one another than those associated with different contexts, even when their objective temporal distance is fixed. Such temporal memory biases are thought to reflect within-event ... ...

    Abstract Adults remember items with shared contexts as occurring closer in time to one another than those associated with different contexts, even when their objective temporal distance is fixed. Such temporal memory biases are thought to reflect within-event integration and between-event differentiation processes that organize events according to their contextual similarities and differences, respectively. Within-event integration and between-event differentiation are hypothesized to differentially rely on binding and control processes, which may develop at different ages. To test this hypothesis, 5- to 12-year-olds and adults (N = 134) studied quartets of image pairs that contained either the same scene (same-context) or different scenes (different-context). Participants remembered same-context items as occurring closer in time by older childhood (7-9 years), whereas different-context items were remembered as occurring farther apart by early adolescence (10-12 years). The differential emergence of these temporal memory biases suggests within-event integration and between-event differentiation emerge at different ages. RESEARCH HIGHLIGHTS: Children are less likely than adults to use contextual information (e.g., location) to organize their continuous experience in memory, as indicated by temporal memory biases. Biases reflecting within-event integration (i.e., remembering elements with a shared context as occurring closer together in time) emerged in late childhood. Biases reflecting between-event differentiation (i.e., remembering elements from different contexts as occurring farther apart in time) emerged in early adolescence. The differential emergence of biases reflecting within-event integration and between-event differentiation suggests they are distinct, yet complementary, processes that support developmental improvements in event memory organization.
    MeSH term(s) Child ; Adult ; Adolescent ; Humans ; Mental Recall ; Memory, Episodic
    Language English
    Publishing date 2023-08-23
    Publishing country England
    Document type Journal Article
    ZDB-ID 2023952-X
    ISSN 1467-7687 ; 1363-755X
    ISSN (online) 1467-7687
    ISSN 1363-755X
    DOI 10.1111/desc.13437
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  6. Article ; Online: Reinstatement of item-specific contextual details during retrieval supports recombination-related false memories.

    Carpenter, Alexis C / Thakral, Preston P / Preston, Alison R / Schacter, Daniel L

    NeuroImage

    2021  Volume 236, Page(s) 118033

    Abstract: Flexible retrieval mechanisms that allow us to infer relationships across events may also lead to memory errors or distortion when details of one event are misattributed to the related event. Here, we tested how making successful inferences alters ... ...

    Abstract Flexible retrieval mechanisms that allow us to infer relationships across events may also lead to memory errors or distortion when details of one event are misattributed to the related event. Here, we tested how making successful inferences alters representation of overlapping events, leading to false memories. Participants encoded overlapping associations ('AB' and 'BC'), each of which was superimposed on different indoor and outdoor scenes that were pre-exposed prior to associative learning. Participants were subsequently tested on both the directly learned pairs ('AB' and 'BC') and inferred relationships across pairs ('AC'). We predicted that when people make a correct inference, features associated with overlapping events may become integrated in memory. To test this hypothesis, participants completed a final detailed retrieval test, in which they had to recall the scene associated with initially learned 'AB' pairs (or 'BC' pairs). We found that the outcome of inference decisions impacted the degree to which neural patterns elicited during detailed 'AB' retrieval reflected reinstatement of the scene associated with the overlapping 'BC' event. After successful inference, neural patterns in the anterior hippocampus, posterior medial prefrontal cortex, and our content-reinstatement region (left inferior temporal gyrus) were more similar to the overlapping, yet incorrect 'BC' context relative to after unsuccessful inference. Further, greater hippocampal activity during inference was associated with greater reinstatement of the incorrect, overlapping context in our content-reinstatement region, which in turn tracked contextual misattributions during detailed retrieval. These results suggest recombining memories during successful inference can lead to misattribution of contextual details across related events, resulting in false memories.
    MeSH term(s) Adult ; Association Learning/physiology ; Brain Mapping ; Female ; Hippocampus/diagnostic imaging ; Hippocampus/physiology ; Humans ; Magnetic Resonance Imaging ; Male ; Memory, Episodic ; Mental Recall/physiology ; Pattern Recognition, Visual/physiology ; Prefrontal Cortex/diagnostic imaging ; Prefrontal Cortex/physiology ; Temporal Lobe/diagnostic imaging ; Temporal Lobe/physiology ; Thinking/physiology ; Young Adult
    Language English
    Publishing date 2021-04-06
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 1147767-2
    ISSN 1095-9572 ; 1053-8119
    ISSN (online) 1095-9572
    ISSN 1053-8119
    DOI 10.1016/j.neuroimage.2021.118033
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  7. Article ; Online: Developmental differences in memory reactivation relate to encoding and inference in the human brain.

    Schlichting, Margaret L / Guarino, Katharine F / Roome, Hannah E / Preston, Alison R

    Nature human behaviour

    2021  Volume 6, Issue 3, Page(s) 415–428

    Abstract: Despite the fact that children can draw on their memories to make novel inferences, it is unknown whether they do so through the same neural mechanisms as adults. We measured memory reinstatement as participants aged 7-30 years learned new, related ... ...

    Abstract Despite the fact that children can draw on their memories to make novel inferences, it is unknown whether they do so through the same neural mechanisms as adults. We measured memory reinstatement as participants aged 7-30 years learned new, related information. While adults brought memories to mind throughout learning, adolescents did so only transiently, and children not at all. Analysis of trial-wise variability in reactivation showed that discrepant neural mechanisms-and in particular, what we interpret as suppression of interfering memories during learning in early adolescence-are nevertheless beneficial for later inference at each developmental stage. These results suggest that while adults build integrated memories well-suited to informing inference directly, children and adolescents instead must rely on separate memories to be individually referenced at the time of inference decisions.
    MeSH term(s) Adolescent ; Adult ; Brain/diagnostic imaging ; Brain/physiology ; Brain Mapping ; Child ; Humans ; Learning/physiology ; Young Adult
    Language English
    Publishing date 2021-11-15
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ISSN 2397-3374
    ISSN (online) 2397-3374
    DOI 10.1038/s41562-021-01206-5
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  8. Article ; Online: Generalization of cognitive maps across space and time.

    Sherrill, Katherine R / Molitor, Robert J / Karagoz, Ata B / Atyam, Manasa / Mack, Michael L / Preston, Alison R

    Cerebral cortex (New York, N.Y. : 1991)

    2023  Volume 33, Issue 12, Page(s) 7971–7992

    Abstract: Prominent theories posit that associative memory structures, known as cognitive maps, support flexible generalization of knowledge across cognitive domains. Here, we evince a representational account of cognitive map flexibility by quantifying how ... ...

    Abstract Prominent theories posit that associative memory structures, known as cognitive maps, support flexible generalization of knowledge across cognitive domains. Here, we evince a representational account of cognitive map flexibility by quantifying how spatial knowledge formed one day was used predictively in a temporal sequence task 24 hours later, biasing both behavior and neural response. Participants learned novel object locations in distinct virtual environments. After learning, hippocampus and ventromedial prefrontal cortex (vmPFC) represented a cognitive map, wherein neural patterns became more similar for same-environment objects and more discriminable for different-environment objects. Twenty-four hours later, participants rated their preference for objects from spatial learning; objects were presented in sequential triplets from either the same or different environments. We found that preference response times were slower when participants transitioned between same- and different-environment triplets. Furthermore, hippocampal spatial map coherence tracked behavioral slowing at the implicit sequence transitions. At transitions, predictive reinstatement of virtual environments decreased in anterior parahippocampal cortex. In the absence of such predictive reinstatement after sequence transitions, hippocampus and vmPFC responses increased, accompanied by hippocampal-vmPFC functional decoupling that predicted individuals' behavioral slowing after a transition. Collectively, these findings reveal how expectations derived from spatial experience generalize to support temporal prediction.
    MeSH term(s) Humans ; Learning ; Hippocampus/physiology ; Cerebral Cortex/physiology ; Prefrontal Cortex/physiology ; Cognition ; Magnetic Resonance Imaging
    Language English
    Publishing date 2023-03-28
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 1077450-6
    ISSN 1460-2199 ; 1047-3211
    ISSN (online) 1460-2199
    ISSN 1047-3211
    DOI 10.1093/cercor/bhad092
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  9. Article ; Online: Ventromedial prefrontal cortex compression during concept learning.

    Mack, Michael L / Preston, Alison R / Love, Bradley C

    Nature communications

    2020  Volume 11, Issue 1, Page(s) 46

    Abstract: Prefrontal cortex (PFC) is thought to support the ability to focus on goal-relevant information by filtering out irrelevant information, a process akin to dimensionality reduction. Here, we test this dimensionality reduction hypothesis by relating a data- ...

    Abstract Prefrontal cortex (PFC) is thought to support the ability to focus on goal-relevant information by filtering out irrelevant information, a process akin to dimensionality reduction. Here, we test this dimensionality reduction hypothesis by relating a data-driven approach to characterizing the complexity of neural representation with a theoretically-supported computational model of learning. We find evidence of goal-directed dimensionality reduction within human ventromedial PFC during learning. Importantly, by using computational predictions of each participant's attentional strategies during learning, we find that that the degree of neural compression predicts an individual's ability to selectively attend to concept-specific information. These findings suggest a domain-general mechanism of learning through compression in ventromedial PFC.
    MeSH term(s) Adolescent ; Adult ; Female ; Goals ; Humans ; Learning ; Magnetic Resonance Imaging ; Male ; Prefrontal Cortex/diagnostic imaging ; Prefrontal Cortex/physiology ; Young Adult
    Language English
    Publishing date 2020-01-07
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2553671-0
    ISSN 2041-1723 ; 2041-1723
    ISSN (online) 2041-1723
    ISSN 2041-1723
    DOI 10.1038/s41467-019-13930-8
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  10. Article ; Online: Semantic Knowledge of Famous People and Places Is Represented in Hippocampus and Distinct Cortical Networks.

    Morton, Neal W / Zippi, Ellen L / Noh, Sharon M / Preston, Alison R

    The Journal of neuroscience : the official journal of the Society for Neuroscience

    2021  Volume 41, Issue 12, Page(s) 2762–2779

    Abstract: Studies have found that anterior temporal lobe (ATL) is critical for detailed knowledge of object categories, suggesting that it has an important role in semantic memory. However, in addition to information about entities, such as people and objects, ... ...

    Abstract Studies have found that anterior temporal lobe (ATL) is critical for detailed knowledge of object categories, suggesting that it has an important role in semantic memory. However, in addition to information about entities, such as people and objects, semantic memory also encompasses information about places. We tested predictions stemming from the PMAT model, which proposes there are distinct systems that support different kinds of semantic knowledge: an anterior temporal (AT) network, which represents information about entities; and a posterior medial (PM) network, which represents information about places. We used representational similarity analysis to test for activation of semantic features when human participants viewed pictures of famous people and places, while controlling for visual similarity. We used machine learning techniques to quantify the semantic similarity of items based on encyclopedic knowledge in the Wikipedia page for each item and found that these similarity models accurately predict human similarity judgments. We found that regions within the AT network, including ATL and inferior frontal gyrus, represented detailed semantic knowledge of people. In contrast, semantic knowledge of places was represented within PM network areas, including precuneus, posterior cingulate cortex, angular gyrus, and parahippocampal cortex. Finally, we found that hippocampus, which has been proposed to serve as an interface between the AT and PM networks, represented fine-grained semantic similarity for both individual people and places. Our results provide evidence that semantic knowledge of people and places is represented separately in AT and PM areas, whereas hippocampus represents semantic knowledge of both categories.
    MeSH term(s) Adult ; Cerebral Cortex/diagnostic imaging ; Cerebral Cortex/physiology ; Famous Persons ; Female ; Hippocampus/diagnostic imaging ; Hippocampus/physiology ; Humans ; Magnetic Resonance Imaging/methods ; Male ; Nerve Net/diagnostic imaging ; Nerve Net/physiology ; Photic Stimulation/methods ; Recognition, Psychology/physiology ; Semantics ; Young Adult
    Language English
    Publishing date 2021-02-05
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 604637-x
    ISSN 1529-2401 ; 0270-6474
    ISSN (online) 1529-2401
    ISSN 0270-6474
    DOI 10.1523/JNEUROSCI.2034-19.2021
    Database MEDical Literature Analysis and Retrieval System OnLINE

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