Functional re-organization of hippocampal-cortical gradients during naturalistic memory processes

Borne, Léonie; Lupton, Michelle K.; Meer, Johan N. van der; Jeganathan, Jayson; Paton, Bryan; Koussis, Nikitas; Guo, Christine; Robinson, Gail; Fripp, Jürgen; Zalesky, Andrew; Breakspear, Michael

doi:10.1016/j.neuroimage.2023.119996

Cited by 15 publications

(19 citation statements)

References 68 publications

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“…Complementing these task-free investigations, the current study derived topographic gradients during episodic and semantic memory states separately, yet it still found that they largely followed similar intrinsic organizational axes 10, 23, 25 . Specifically, connectivity patterns during both memory states followed topographic gradients including a sensory-transmodal neocortical and posterior-anterior hippocampal pattern, which are in line with previous observations 63, 68, 69, 72–74 . Transmodal core regions ( i.e., DMN) occupy a cortical territory that is maximally distant and separate from unimodal sensory systems, balancing segregated processing streams and integration 64, 66,63, 64, 99 .…”

Section: Discussionsupporting

confidence: 90%

Differential Reorganization of Episodic and Semantic Memory Systems in Epilepsy-Related Mesiotemporal Pathology

Cabalo,

DeKraker,

Royer

et al. 2023

Preprint

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Declarative memory encompasses episodic and semantic divisions. Episodic memory captures singular events with specific spatiotemporal relationships, while semantic memory houses context-independent knowledge. Behavioral and functional neuroimaging studies have revealed common and distinct neural substrates of both memory systems, implicating mesiotemporal lobe (MTL) regions and distributed neocortices. Here, we studied a population of patients with unilateral temporal lobe epilepsy (TLE) and variable degrees of MTL pathology as a human disease model to explore declarative memory system reorganization, and to examine neurocognitive associations. Our cohort included 20 patients with TLE as well as 60 age and sex-matched healthy controls, who underwent episodic and semantic retrieval tasks during a functional MRI session. Tasks were closely matched in terms of stimuli and trial design. Capitalizing on connectome gradient mapping techniques, we derived task-based functional topographies during episodic and semantic memory states, both in the MTL and in neocortical networks. Comparing neocortical and hippocampal functional gradients between TLE patients and healthy controls, we observed topographic reorganization during episodic but not semantic memory states, characterized by marked gradient compression in lateral temporal and midline parietal cortices in both hemispheres, cooccurring with an expansion of anterior-posterior hippocampal differentiation ipsilateral to the MTL pathology. These findings suggest that episodic processes are supported by a distributed network, implicating both hippocampus and neocortex, and such alterations can provide a compact signature of state-dependent reorganization in conditions associated with MTL damage such as TLE. Leveraging microstructural and morphological MRI proxies of MTL pathology, we furthermore observed that pathological markers selective to the hippocampus are associated with TLE-related functional reorganization. Moreover, correlation analysis and statistical mediation models revealed that these functional alterations contributed to behavioral deficits in episodic memory in patients. Altogether, our findings point to a selective mesiotemporal and neocortical functional reorganization of episodic memory systems in patients with TLE, which consistently affects behavioral memory deficits. These findings point to consistent structure-function relationships in declarative memory and reaffirm the critical role of the MTL in episodic memory systems.

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Section: Discussionsupporting

confidence: 90%

Differential Reorganization of Episodic and Semantic Memory Systems in Epilepsy-Related Mesiotemporal Pathology

Cabalo,

DeKraker,

Royer

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…For example, maps of hippocampal cyto-or myeloarchitectonic features can be constructed from multiple samples using different stains or imaging methods that would otherwise preclude one another due to tissue destruction (e.g., once stained, a slice cannot be easily imaged with other stains). This can be useful both in studying hippocampal subfields and in subfield-agnostic mapping and other data driven methods (e.g., Borne et al, 2023;Paquola et al, 2020;Patel et al, 2020;Przeździk et al, 2019;Vogel et al, 2020;Vos de Wael et al, 2018). We hope that this work will provide an avenue towards mapping of hippocampal data across many modalities, scales, and different fields in future work.…”

Section: Discussionmentioning

confidence: 96%

“…This can be useful both in studying hippocampal subfields and in subfield-agnostic mapping and other data driven methods ( e . g ., Borne et al, 2023; Paquola et al, 2020; Patel et al, 2020; Przeździk et al, 2019; Vogel et al, 2020; Vos de Wael et al, 2018). We hope that this work will provide an avenue towards mapping of hippocampal data across many modalities, scales, and different fields in future work.…”

Section: Discussionmentioning

confidence: 99%

Evaluation of surface-based hippocampal registration using ground-truth subfield definitions

DeKraker

Palomero-Gallagher

Kedo

et al. 2023

Preprint

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The hippocampus is an archicortical structure, consisting of subfields with unique circuits. Understanding its microstructure, as proxied by these subfields, can improve our mechanistic understanding of learning and memory and has clinical potential for several neurological disorders. One prominent issue is how to parcellate, register, or retrieve homologous points between two hippocampi with grossly different morphologies. Here, we present a surface-based registration method that solves this issue in a contrast-agnostic, topology-preserving manner. Specifically, the entire hippocampus is first analytically unfolded, and then samples are registered in 2D unfolded space based on thickness, curvature, and gyrification. We demonstrate this method in seven 3D histology samples and show superior alignment with respect to subfields using this method over more conventional registration approaches.

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“…The topological distribution of amyloid PET binding has been shown to overlap with the “default mode” resting state network 69 . Evidence is emerging from analyses of functional gradients within the hippocampus and the cortical mantle that the default mode network may show the strongest hippocampal connectivity at the transition between the head and body 70 . This has relevant implications for the understanding of clinical manifestations and progression of AD.…”

Section: Discussionmentioning

confidence: 99%

Three‐dimensional histology reveals dissociable human hippocampal long‐axis gradients of Alzheimer's pathology

Ortega‐Cruz,

Bress,

Gazula

et al. 2024

Alzheimer's & Dementia

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INTRODUCTIONThree‐dimensional (3D) histology analyses are essential to overcome sampling variability and understand pathological differences beyond the dissection axis. We present Path2MR, the first pipeline allowing 3D reconstruction of sparse human histology without a magnetic resonance imaging (MRI) reference. We implemented Path2MR with post‐mortem hippocampal sections to explore pathology gradients in Alzheimer's disease.METHODSBlockface photographs of brain hemisphere slices are used for 3D reconstruction, from which an MRI‐like image is generated using machine learning. Histology sections are aligned to the reconstructed hemisphere and subsequently to an atlas in standard space.RESULTSPath2MR successfully registered histological sections to their anatomic position along the hippocampal longitudinal axis. Combined with histopathology quantification, we found an expected peak of tau pathology at the anterior end of the hippocampus, whereas amyloid‐beta (Aβ) displayed a quadratic anterior‐posterior distribution.CONCLUSIONPath2MR, which enables 3D histology using any brain bank data set, revealed significant differences along the hippocampus between tau and Aβ.Highlights Path2MR enables three‐dimensional (3D) brain reconstruction from blockface dissection photographs. This pipeline does not require dense specimen sampling or a subject‐specific magnetic resonance (MR) image. Anatomically consistent mapping of hippocampal sections was obtained with Path2MR. Our analyses revealed an anterior‐posterior gradient of hippocampal tau pathology. In contrast, the peak of amyloid‐beta (Aβ) deposition was closer to the hippocampal body.

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Functional re-organization of hippocampal-cortical gradients during naturalistic memory processes

Cited by 15 publications

References 68 publications

Differential Reorganization of Episodic and Semantic Memory Systems in Epilepsy-Related Mesiotemporal Pathology

Differential Reorganization of Episodic and Semantic Memory Systems in Epilepsy-Related Mesiotemporal Pathology

Evaluation of surface-based hippocampal registration using ground-truth subfield definitions

Three‐dimensional histology reveals dissociable human hippocampal long‐axis gradients of Alzheimer's pathology

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