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Coherence and congruency mediate medial temporal and medial prefrontal activity during event construction
Abstract
The precise roles of the hippocampus (HPC) and medial prefrontal cortex (mPFC) in initially constructing imagined events remains unclear. HPC activity during imagination may be modulated by mnemonic load, given its role in working memory for complex materials, and/or by the semantic relatedness (i.e. congruency) between items and their context. MPFC activation may track with congruency or mnemonic load, given the role of ventral mPFC in schema processing and the dorsal mPFC in working memory for social information. Sixteen healthy adults (M age = 22.3) underwent an event construction task, wherein participants were provided with a context and item words and imagined an event, forming as many inter-item associations as possible among the items. The stimuli varied by set size and by normatively-defined congruence (normative congruency) to explore their effects on HPC and mPFC activity and functional connectivity. We observed HPC connectivity during event construction in general, whereas dorsal mPFC connectivity occurred during imagining only at higher set sizes. Moreover, anterior hippocampal activity correlated positively with increasing coherence between items during imagining, suggesting that the anterior HPC is sensitive to the relational demands of constructing a novel event. Parahippocampal, hippocampal, temporal pole, and mPFC activity tracked only with individual differences in subjective ratings of congruency of imagined events, which may contribute to construction by retrieving existing schema-related information. Collectively, these findings provide new insights into the factors that modulate HPC and mPFC activity when constructing mental simulations.
... rabbit and dog are both animals). Previous research has provided evidence that semantic relationships are represented in the hippocampus (Romero et al. 2019;Solomon et al. 2019;Pacheco Estefan et al. 2021) but also across various cortical regions (Charest et al. 2014;Clarke and Tyler 2014;Bracci et al. 2015;Price et al. 2015;Huth et al. 2016;Frisby et al. 2023). ...
... Our finding that object relationships are represented in the hippocampus is also consistent with previous findings that the hippocampus is involved in the retrieval of semantic memory, particularly for relational knowledge between concepts, and that hippocampal activity ref lects distances in semantic spaces (Pacheco Estefan et al. 2021;Romero et al. 2019;Solomon et al. 2019). The hippocampus thus seems to support domain-general processing of semantic knowledge (Staresina et al. 2011;Ranganath and Ritchey 2012;Morton et al. 2021). ...
The hippocampal-entorhinal system uses cognitive maps to represent spatial knowledge and other types of relational information. However, objects can often be characterized by different types of relations simultaneously. How does the hippocampal formation handle the embedding of stimuli in multiple relational structures that differ vastly in their mode and timescale of acquisition? Does the hippocampal formation integrate different stimulus dimensions into one conjunctive map or is each dimension represented in a parallel map? Here, we reanalyzed human functional magnetic resonance imaging data from Garvert et al. (2017) that had previously revealed a map in the hippocampal formation coding for a newly learnt transition structure. Using functional magnetic resonance imaging adaptation analysis, we found that the degree of representational similarity in the bilateral hippocampus also decreased as a function of the semantic distance between presented objects. Importantly, while both map-like structures localized to the hippocampal formation, the semantic map was located in more posterior regions of the hippocampal formation than the transition structure and thus anatomically distinct. This finding supports the idea that the hippocampal-entorhinal system forms parallel cognitive maps that reflect the embedding of objects in diverse relational structures.
... It is well known that prefrontal-hippocampal interactions mediate episodic memory and spatial navigation [7,[41][42][43][44][45][46]. Recent human and animal studies suggest that the DLPFC and hippocampus are also involved in sequential working memory. ...
The prefrontal cortex and hippocampus may support sequential working memory beyond episodic memory and spatial navigation. This stereoelectroencephalography (SEEG) study investigated how the dorsolateral prefrontal cortex (DLPFC) interacts with the hippocampus in the online processing of sequential information. Twenty patients with epilepsy (eight women, age 27.6 ± 8.2 years) completed a line ordering task with SEEG recordings over the DLPFC and the hippocampus. Participants showed longer thinking times and more recall errors when asked to arrange random lines clockwise (random trials) than to maintain ordered lines (ordered trials) before recalling the orientation of a particular line. First, the ordering-related increase in thinking time and recall error was associated with a transient theta power increase in the hippocampus and a sustained theta power increase in the DLPFC (3–10 Hz). In particular, the hippocampal theta power increase correlated with the memory precision of line orientation. Second, theta phase coherences between the DLPFC and hippocampus were enhanced for ordering, especially for more precisely memorized lines. Third, the theta band DLPFC → hippocampus influence was selectively enhanced for ordering, especially for more precisely memorized lines. This study suggests that theta oscillations may support DLPFC-hippocampal interactions in the online processing of sequential information.
... Recent studies 23,27,68 , including the current study, thus extend the framework by differentiating the involvement of the hippocampus subregions and vmPFC-lateral PFC connectivity in PK-related processing. When a memory retrieval begins, the vmPFC, as a schema detector, is responsible for activating the appropriate context during schema reinstatement and instantiation through biasing posterior neocortical regions representing the exemplars related to appropriate PK 33,113,114 . At this stage, the coupling of the vmPFC-amHPC, and vmPFC-PRC/ ITG may be more involved in retrieving gist-based information or the information with high PK 28,91 . ...
Previous studies have shown that the ventral medial prefrontal cortex (vmPFC) plays an important role in schema-related memory. However, there is an intensive debate to what extent the activation of subregions of the hippocampus is involved in retrieving schema-related memory. In addition, it is unclear how the functional connectivity (FC) between the vmPFC and the hippocampus, as well as the connectivity of the vmPFC with other regions, are modulated by prior knowledge (PK) during memory retrieval over time. To address these issues, participants learned paragraphs that described features of each unfamiliar word from familiar and unfamiliar categories (i.e., high and low PK conditions) 20 min, 1 day, and 1 week before the test. They then performed a recognition task to judge whether the sentences were old in the scanner. The results showed that the activation of the anterior-medial hippocampus (amHPC) cluster was stronger when the old sentences with high (vs. low) PK were correctly retrieved. The activation of the posterior hippocampus (pHPC) cluster, as well as the vmPFC, was stronger when the new sentences with high (vs. low) PK were correctly rejected (i.e., CR trials), whereas the cluster of anterior-lateral hippocampus (alHPC) showed the opposite. The FC of the vmPFC with the amHPC and perirhinal cortex/inferior temporal gyrus was stronger in the high (vs. low) PK condition, whereas the FC of the vmPFC with the alHPC, thalamus and frontal regions showed the opposite for the CR trials. This study highlighted that different brain networks, which were associated with the vmPFC, subregions of the hippocampus and cognitive control regions, were responsible for retrieving the information with high and low PK.
... Notably, the same hippocampal-vmPFC interactions implicated in concept learning (Kumaran et al., 2009;Bowman and Zeithamova, 2018;Frank et al., 2019) have been implicated in memory integration and inference in both neuroimaging (Zeithamova et al., 2012; and lesion work (Dusek and Eichenbaum, 1997;Ryan et al., 2016;Spalding et al., 2018). Finally, the same regions have been shown to underlie schema-related memory (Tse et al., 2007(Tse et al., , 2011van Kesteren et al., 2012;Spalding et al., 2015;Brod et al., 2017;Gilboa and Marlatte, 2017;Gilboa and Moscovitch, 2017;Baldassano et al., 2018;Romero et al., 2019). Thus, hippocampal-vmPFC memory integration mechanisms may serve to link related information to a coherent representation in service of a range of generalization tasks, including concept learning. ...
Concept learning, the ability to extract commonalities and highlight distinctions across a set of related experiences to build organized knowledge, is a critical aspect of cognition. Previous reviews have focused on concept learning research as a means for dissociating multiple brain systems. The current review surveys recent work that uses novel analytical approaches, including the combination of computational modeling with neural measures, focused on testing theories of specific computations and representations that contribute to concept learning. We discuss in detail the roles of the hippocampus, ventromedial prefrontal, lateral prefrontal, and lateral parietal cortices, and how their engagement is modulated by the coherence of experiences and the current learning goals. We conclude that the interaction of multiple brain systems relating to learning, memory, attention, perception, and reward support a flexible concept-learning mechanism that adapts to a range of category structures and incorporates motivational states, making concept learning a fruitful research domain for understanding the neural dynamics underlying complex behaviors.
... The hippocampus, and its connections, which is an influential structure in regards to episodic memory and schematic representation, is one of two structures, with the medial prefrontal cortex, the most involved in the construction of events or scenes that underlies the imagination (Romero, Barense & Moscovitch, 2019). ...
According to the enactive approach to the mind, we enact the world mentally through our interactions with it (Thompson, 2010; Varela et al., 1991, Maturana & Varela, 1987). Moreover, according to Andy Clark (2016), our brain is active all the time, dashing off thousands of predictions of what we might encounter and thus preparing our body to deal with it. As a consequence, our brain processes most of the time more inputs from itself than from the outside world (Feldman Barrett, 2017; Seth, 2015; Hohwy, 2013). But not only the structure of our reality is built from an intrinsic brain activity that call on prior knowledge that experience has laid down in our synaptic connections, it is also tinged by the fictional narratives (Vaihinger, 1911) that take shape through our affordances and our conceptual inferences.
How do these ideas translate when we focus on a sensory system in particular? Numerous odorous harmonies occupy the environment, which, when captured by our olfactory system, allow us to evolve, by conscious or distracted mental projection, between the virtual planes of innumerable places encoded in our memory (Eichenbaum., 2017). I call these odorous harmonies olfactory ambiances. Olfactory ambiances affect our olfactory memory, which in turn affects three important aspects our mental live: spatiotemporal patterns, the emotional valence associated with these patterns, and our olfactory experience of the world, which I call its “smellscape.”
The hippocampal-entorhinal system uses cognitive maps to represent spatial knowledge and other types of relational information, such as the transition probabilities between objects. However, objects can often be characterized in terms of different types of relations simultaneously, e.g. semantic similarities learned over the course of a lifetime as well as transitions experienced over a brief timeframe in an experimental setting. Here we ask how the hippocampal formation handles the embedding of stimuli in multiple relational structures that differ vastly in terms of their mode and timescale of acquisition: Does it integrate the different stimulus dimensions into one conjunctive map, or is each dimension represented in a parallel map? To this end, we reanalyzed functional magnetic resonance imaging (fMRI) data from Garvert et al. (2017) that had previously revealed an entorhinal map which coded for newly learnt statistical regularities. We used a triplet odd-one-out task to construct a semantic distance matrix for presented items and applied fMRI adaptation analysis to show that the degree of similarity of representations in bilateral hippocampus decreases as a function of semantic distance between presented objects. Importantly, while both maps localize to the hippocampal formation, this semantic map is anatomically distinct from the originally described entorhinal map. This finding supports the idea that the hippocampal-entorhinal system forms parallel cognitive maps reflecting the embedding of objects in diverse relational structures.
Memory-based cognition depends on both the ability to remember specific details of individual experiences and the ability to combine information across experiences to generalize and derive new knowledge. A hippocampal role in rapid encoding of specific events is long established. More recent research also demonstrates hippocampal contributions to generalization, but their nature is still debated. The current review provides an overview of hippocampal-based generalization in two lines of research—episodic inference and categorization—and discusses evidence for four candidate mechanisms and representational schemes that may underpin such generalization. We highlight evidence showing that the hippocampus contributes specific memories to generalization decisions, but also forms generalized representations that integrate information across experiences. Multiple views are currently plausible of how such generalized representations form and relate to specific memories. Future research that uses behavioral and neural indices of both generalization and specificity may help resolve between the candidate generalization mechanisms, with the possibility that more than one view of hippocampal-based generalization may be valid. Importantly, all views share the emphasis on the broader role of the hippocampus in cognition that goes beyond remembering the past.
It has been argued that the hippocampus supports cognition by virtue of its role in flexibly binding together distinct elements of experience. Such ‘relational processing’ enables us to (re)construct episodic representations of real or imagined events. The present study examined whether hippocampally mediated relational processing also contributes to the construction of semantic representations. To do so, we asked amnesic individuals with medial temporal lobe (MTL) lesions including the hippocampus to generate hypothetical meanings for novel word compounds (e.g., cactus carpet), a task that requires existing concepts to be flexibly linked. The quality of definitions and number of features generated for the novel compounds were lower in patients with MTL lesions than in control participants. Whereas the subset of patients with lesions extending into lateral temporal cortex had additional difficulty generating meanings for pre‐existing compounds (e.g., bus station), patients with lesions limited to the MTL showed no such deficit, indicating that their impairment in the novel compound condition was not due to reduced access to semantic information. These findings suggest that the role of hippocampally mediated relational processing extends beyond the episodic domain to include the generation of novel semantic representations.
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