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Time-dependent memory transformation along the hippocampal anterior-posterior axis.

ABSTRACT: With time, memories undergo a neural reorganization that is linked to a transformation of detailed, episodic into more semantic, gist-like memory. Traditionally, this reorganization is thought to involve a redistribution of memory from the hippocampus to neocortical areas. Here we report a time-dependent reorganization within the hippocampus, along its anterior-posterior axis, that is related to the transformation of detailed memories into gist-like representations. We show that mnemonic representations in the anterior hippocampus are highly distinct and that anterior hippocampal activity is associated with detailed memory but decreases over time. Posterior hippocampal representations, however, are more gist-like at a later retention interval, and do not decline over time. These findings indicate that, in addition to the well-known systems consolidation from hippocampus to neocortex, there are changes within the hippocampus that are crucial for the temporal dynamics of memory.

SUBMITTER: Dandolo LC

PROVIDER: S-EPMC5865114 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Time-dependent memory transformation along the hippocampal anterior-posterior axis.

Dandolo Lisa C LC Schwabe Lars L

Nature communications 20180323 1

With time, memories undergo a neural reorganization that is linked to a transformation of detailed, episodic into more semantic, gist-like memory. Traditionally, this reorganization is thought to involve a redistribution of memory from the hippocampus to neocortical areas. Here we report a time-dependent reorganization within the hippocampus, along its anterior-posterior axis, that is related to the transformation of detailed memories into gist-like representations. We show that mnemonic represe ...[more]

PMID: 29572516

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Project description:While age-related volumetric changes in human hippocampal subfields have been reported, little is known about patterns of subfield functional connectivity (FC) in the context of healthy ageing. Here we investigated age-related changes in patterns of FC down the anterior-posterior axis of each subfield. Using high resolution structural MRI we delineated the dentate gyrus (DG), CA fields (including separating DG from CA3), the subiculum, pre/parasubiculum, and the uncus in healthy young and older adults. We then used high resolution resting state functional MRI to measure FC in each group and to directly compare them. We first examined the FC of each subfield in its entirety, in terms of FC with other subfields and with neighboring cortical regions, namely, entorhinal, perirhinal, posterior parahippocampal, and retrosplenial cortices. Next, we analyzed subfield to subfield FC within different portions along the hippocampal anterior-posterior axis, and FC of each subfield portion with the neighboring cortical regions of interest. In general, the FC of the older adults was similar to that observed in the younger adults. We found that, as in the young group, the older group displayed intrinsic FC between the subfields that aligned with the tri-synaptic circuit but also extended beyond it, and that FC between the subfields and neighboring cortical areas differed markedly along the anterior-posterior axis of each subfield. We observed only one significant difference between the young and older groups. Compared to the young group, the older participants had significantly reduced FC between the anterior CA1-subiculum transition region and the transentorhinal cortex, two brain regions known to be disproportionately affected during the early stages of age-related tau accumulation. Overall, these results contribute to ongoing efforts to characterize human hippocampal subfield connectivity, with implications for understanding hippocampal function and its modulation in the ageing brain.

Project description:Neurological symptoms following cerebellar stroke can range from motor to cognitive-affective impairments. Topographic imaging studies from patients with lesions confined to the cerebellum have shown evidence linking anterior cerebellar lobules with motor function and posterior lobules with cognitive function. Damage to the cerebellum can disrupt functional connectivity in cerebellar stroke patients, as it is highly interconnected with forebrain motor and cognitive areas. The hippocampus plays a key role in memory acquisition, a cognitive domain that is negatively impacted by posterior cerebellar stroke, and there is increasing evidence that the cerebellum can affect hippocampal function in health and disease. To study these topographical dissociations, we developed a mouse photo-thrombosis model to produce unilateral strokes in anterior (lobules III-V) or posterior (lobules VI-VIII) cerebellar cortex to examine hippocampal plasticity and behavior. Histological and MRI data demonstrate reproducible injury that is confined to the targeted lobules. We then measured hippocampal long-term potentiation (LTP) ex-vivo with extracellular field recording experiments in acute brain slices obtained from mice 7 days post-cerebellar stroke. Interestingly, we found that a unilateral posterior stroke resulted in a contralateral hippocampal impairment, matching the cerebellothalamic pathway trajectory, while LTP was intact in both hippocampi of mice with anterior strokes. We also assessed motor coordination and memory function at 7 days post-stroke using a balance beam, contextual and delay fear conditioning (CFC and DFC), and novel object recognition (NOR) tasks. Mice with anterior strokes showed lack of coordination evaluated as an increased number of missteps, while mice with posterior strokes did not. Mice with anterior or posterior cerebellar strokes demonstrated similar freezing behavior to shams in CFC and DFC, while only posterior stroke mice displayed a reduced discrimination index in the NOR task. These data suggest that a unilateral LTP impairment observed in mice with posterior strokes produces a mild memory impairment. Our results demonstrate that our model recapitulates aspects of clinical lesion-symptom mapping, with anterior cerebellar strokes producing impaired motor coordination and posterior cerebellar strokes producing an object-recognition memory impairment. Further studies are warranted to interrogate other motor and cognitive-affective behaviors and brain region specific alterations following focal cerebellar stroke. The novel model presented herein will allow for future preclinical translational studies to improve neurological deficits after cerebellar stroke.

Dataset Information

Time-dependent memory transformation along the hippocampal anterior-posterior axis.

Publications

Time-dependent memory transformation along the hippocampal anterior-posterior axis.

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