Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4T

Mueller, Susanne; Chao, Li-Lian; Berman, Brian D.; Weiner, Michael W.

doi:10.1016/j.neuroimage.2011.03.028

Cited by 124 publications

(135 citation statements)

References 55 publications

(69 reference statements)

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“…However, supplemental analyses revealed that CA1-SP thickness also was positively associated with performance. This finding extends prior work from our laboratory demonstrating positive correlations between both layers of CA1 and memory in mild AD (45), as well as other research showing a relationship between atrophy of CA1 and memory impairment in individuals with MCI (43,44). Although some studies of aging and mild AD have reported selective atrophy of DG/ CA3 or subiculum (11), our supplemental analysis of DG/CA3 area revealed nonsignificant findings, and we did not measure subiculum size in this study.…”

Section: Discussionsupporting

confidence: 86%

Individual differences in associative memory among older adults explained by hippocampal subfield structure and function

Carr

Bernstein

Favila

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Older adults experience impairments in episodic memory, ranging from mild to clinically significant. Given the critical role of the medial temporal lobe (MTL) in episodic memory, age-related changes in MTL structure and function may partially account for individual differences in memory. Using ultra-high-field 7T structural MRI and high-resolution 3T functional MRI (hr-fMRI), we evaluated MTL subfield thickness and function in older adults representing a spectrum of cognitive health. Participants performed an associative memory task during hr-fMRI in which they encoded and later retrieved face-name pairs. Motivated by prior research, we hypothesized that differences in performance would be explained by the following: (i) entorhinal cortex (ERC) and CA1 apical neuropil layer [CA1-stratum radiatum lacunosum moleculare (SRLM)] thickness, and (ii) activity in ERC and the dentate gyrus (DG)/CA3 region. Regression analyses revealed that this combination of factors significantly accounted for variability in memory performance. Among these metrics, CA1-SRLM thickness was positively associated with memory, whereas DG/CA3 retrieval activity was negatively associated with memory. Furthermore, including structural and functional metrics in the same model better accounted for performance than did single-modality models. These results advance the understanding of how independent but converging influences of both MTL subfield structure and function contribute to age-related memory impairment, complementing findings in the rodent and human postmortem literatures.episodic memory | hippocampus | aging | mild cognitive impairment | Alzheimer's disease E pisodic memory, or the capacity to encode and subsequently retrieve memories for events, is known to be particularly vulnerable to age-related change (1-3). Older adults show varying degrees of episodic memory impairment, ranging from mild to clinically significant. One potential factor underlying such differences is variability in the structure and function of the medial temporal lobe (MTL).The MTL is essential for episodic memory (4-7), and research across species indicates that the MTL changes in both healthy aging and in age-related neurodegenerative disease (for reviews, see refs. 8 and 9). Critically, however, the MTL is not a unitary structure. Rather, it is composed of multiple regions with differing anatomy and connectivity (see, e.g., ref. 10), including subfields of the hippocampal formation [CA1, CA2, CA3, dentate gyrus (DG), and subiculum], and the entorhinal (ERC), perirhinal (PRC), and parahippocampal (PHC) cortices (Fig. 1A). Moreover, evidence in rodents and humans suggests that these subfields are differentially affected by age, as well as by age-related disease (8, 9, 11).Converging evidence in human studies of healthy aging using high-resolution magnetic resonance imaging (MRI) suggests disproportionate age-related atrophy in CA1 (12-15), although some studies point to selective atrophy of the subiculum or DG/CA3, while others suggest changes encompassing multip...

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Section: Discussionsupporting

confidence: 86%

Individual differences in associative memory among older adults explained by hippocampal subfield structure and function

Carr

Bernstein

Favila

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Recent high-resolution volumetry did show an association between CA1 volume and episodic memory retrieval (38). The impairment of autobiographical memory retrieval during the acute TGA thus mirrors a profound but transient impairment of CA1-dependent hippocampal function leading to an acute diaschisis and reduced connectivity within this network.…”

Section: Discussionmentioning

confidence: 90%

CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness

Bartsch¹,

Döhring²,

Rohr

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

227

159

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Autobiographical memories in our lives are critically dependent on temporal lobe structures. However, the contribution of CA1 neurons in the human hippocampus to the retrieval of episodic autobiographical memory remains elusive. In patients with a rare acute transient global amnesia, highly focal lesions confined to the CA1 field of the hippocampus can be detected on MRI. We studied the effect of these lesions on autobiographical memory using a detailed autobiographical interview including the remember/know procedure. In 14 of 16 patients, focal lesions in the CA1 sector of the hippocampal cornu ammonis were detected. Autobiographical memory was significantly affected over all time periods, including memory for remote periods. Impairment of episodic memory and autonoetic consciousness exhibited a strong temporal gradient extending 30 to 40 y into the past. These results highlight the distinct and critical role of human hippocampal CA1 neurons in autobiographical memory retrieval and for re-experiencing detailed episodic memories.A utobiographical memory is one of the multifaceted forms of human memory that constitutes a major source for selfidentity, self-continuity, and self-awareness of an individual's life. Episodic autobiographical recollection includes conscious awareness for specific episodic situations embedded in time and space, and the ability of mental reliving of episodes of a person's history along the subjective and mental time axis (1). Considering the phenomenological experience of remembering, episodic recollection involving re-experiencing requires autonoetic consciousness in contrast to semantic knowledge of memory, which is associated with noetic consciousness (2).It is generally accepted that the hippocampus plays a critical role in episodic memory, including autobiographical memory, as neuroimaging data show hippocampal activation in autobiographical memory retrieval tasks, supporting that the hippocampus is an integral structure of the autobiographical network (3, 4). The involvement of the hippocampus culminates in the question of the temporal contribution of the hippocampal-neocortical interaction in the consolidation and recollection of remote episodic memory (5). One view, according to the standard model of consolidation, considers the hippocampus as a temporary relay structure that facilitates the transition of newly encoded hippocampus-dependant memory traces to its permanent storage and consolidation in neocortical structures, resulting in hippocampus-independent remote memories (6). This transitory role of the hippocampus is thought to be reflected in the temporal gradient of retrograde amnesia seen in patients with lesions to the medial temporal lobe (MTL). Evidence for this time-limited role of the hippocampus has come from lesion studies of amnestic patients and neuroimaging studies (7,8). In contrast, the multiple trace theory (MTT) postulates a permanent contribution of the hippocampus in retrieving and recollection in terms of a binding module for episodic memories (9). This v...

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“…Moreover, neuronal activity within specific subfields of the hippocampus might serve distinct aspects of memory encoding and retrieval (reviewed in Mueller et al, 2011;Squire, 2004). Therefore, subfield-specific effects of KIBRA genotype might further underline a proposed role for KIBRA genotype in particular aspects of memory formation.…”

Section: Functional Implications and Underlying Mechanismsmentioning

confidence: 99%

Impact of KIBRA Polymorphism on Memory Function and the Hippocampus in Older Adults

Witte

Köbe

Kerti

et al. 2015

Neuropsychopharmacol

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The single nucleotide polymorphism rs17070145 within the KIBRA gene (kidney and brain expressed protein) has been associated with variations in memory functions and related brain areas. However, previous studies yielded conflicting results, which might be due to divergent sample characteristics or task-specific effects. Therefore, we aimed to determine the impact of KIBRA genotype on learning and memory formation, and volume, microstructural integrity and functional connectivity (FC) of the hippocampus and its subfields in a wellcharacterized cohort of healthy older adults. One-hundred and forty subjects (72 women, age 50-80) were KIBRA genotyped and memory was tested using the Auditory Verbal Learning Task. Also, subjects underwent structural and resting-state functional magnetic resonance imaging at 3T. Subfields were delineated using automated segmentation (FreeSurfer software). Microstructural integrity was measured using mean diffusivity (MD) derived from diffusion tensor images. Seed-based analyses were used to assess FC patterns of the hippocampus. KIBRA T-allele carriers showed a trend for better memory performance, and in the hippocampus significantly higher volumes and partly lower MD, indicative for better microstructure, compared with non-T-allele carriers in the cornu ammonis (CA)2/3 and CA4/dentate gyrus subfields (all P ⩽ 0.008, Bonferroni corrected). Also, T-allele carriers exhibited lower FC of the left hippocampus with areas outside the synchronized HC network. In sum, we could show for the first time that older T-allele carriers exhibited larger volumes and better microstructure within those hippocampus subfields that are implicated in long-term potentiation and neurogenesis, key features of memory processes. Moreover, T-allele carriers showed a more selective FC network of the hippocampus.

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Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4T

Cited by 124 publications

References 55 publications

Individual differences in associative memory among older adults explained by hippocampal subfield structure and function

Individual differences in associative memory among older adults explained by hippocampal subfield structure and function

CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness

Impact of KIBRA Polymorphism on Memory Function and the Hippocampus in Older Adults

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