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Aging Along the Hippocampal Axis: Structure, Function and Whole-brain Connections in Association with Memory
Uppsala University, Disciplinary Domain of Humanities and Social Sciences, Faculty of Social Sciences, Department of Psychology.
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Hippocampus-dependent functions display marked reductions in older age, an observation that has led to the extensive study of age effects on hippocampal properties. Even though research indicates that the hippocampus is structurally and functionally heterogeneous along its longitudinal axis, its anterior and posterior regions differentially supporting episodic and spatial memory representations, few studies explicitly consider age effects in relation to axis. Relatedly, as men and women commonly differ in episodic and spatial memory performance, and sometimes also in rates of age-related hippocampal atrophy, sex could be a potential modifier of age effects. The aim of this thesis was therefore to assess age effects on the hippocampus and its role in episodic and spatial memory across young (20-35 years), middle-aged (40-50 years) and older (60-70 years) adults, adopting a longitudinal-axis approach while considering interactions with sex. Study I evaluated hippocampal volume and activation in relation to associative memory across middle-aged and older adults. Age differences in associative memory were largest in men and paralleled by smaller volumes and less activation in the anterior hippocampus. Study II assessed hippocampus-dependent network-like organization of gray matter by measures of structural whole-brain covariance. The anterior and posterior hippocampus showed shared and distinct patterns of covariance, which were qualitatively comparable across age groups. However, participants’ expression of these patterns decreased as a function of age, comparably for men and women, and showed significant associations with episodic memory. Study III investigated age effects on resting-state functional connectivity and demonstrated that both the anterior and posterior hippocampus decreased in connectivity with several brain regions across middle-aged and older adults. Memory was only associated with age-related connectivity of the posterior hippocampus: episodic memory negatively with connectivity increasing as a function of age, and spatial memory positively with connectivity that decreased. These studies demonstrate distinct effects of age on the anterior and posterior hippocampus, and show that age-related decline of these regions differentially relates to episodic and spatial memory. Overall, findings highlight the importance of explicitly considering the heterogeneity of the hippocampal axis in the assessment of its role in age-related memory decline.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2018. , p. 79
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Social Sciences, ISSN 1652-9030 ; 154
Keywords [en]
hippocampus, aging, longitudinal-axis, episodic memory, spatial memory, connectivity, fMRI
National Category
Psychology
Research subject
Psychology
Identifiers
URN: urn:nbn:se:uu:diva-348686ISBN: 978-91-513-0339-0 (print)OAI: oai:DiVA.org:uu-348686DiVA, id: diva2:1198203
Public defence
2018-06-08, Auditorium Minus, Museum Gustavianum, Akademigatan 3, Uppsala, 14:15 (English)
Opponent
Supervisors
Available from: 2018-05-14 Created: 2018-04-17 Last updated: 2018-10-08
List of papers
1. Overlapping effects of age on associative memory and the anterior hippocampus from middle to older age
Open this publication in new window or tab >>Overlapping effects of age on associative memory and the anterior hippocampus from middle to older age
2017 (English)In: Behavioural Brain Research, ISSN 0166-4328, E-ISSN 1872-7549, Vol. 317, p. 350-359Article in journal (Refereed) Published
Abstract [en]

The anterior hippocampus has been implicated in associative memory, and along with hippocampal volume, this type of memory declines with age. However, few cross-sectional studies include middle-aged samples, making it unclear at what point these age-related changes occur. In addition, although men and women have been shown to differ in associative memory and rates of age-related hippocampal atrophy, sex-differences in aging are rarely studied. To address these issues, we assessed memory for word-pairs, hippocampal volume and activation during encoding and retrieval, across middle-aged (n=39) and older (n=44) participants, specifically in relation to sex. Older adults showed significantly poorer associative memory compared to middle-aged adults, paralleled by smaller anterior hippocampi and less activation during successful retrieval. The age-by-sex interaction observed in memory performance was also mirrored in the volume and activation of the hippocampus, indicating more pronounced age-effects in men as compared to women. These results indicate a specific role of the anterior hippocampus in verbal associative memory and suggest they both decline between middle-age and older age.

Keywords
Aging, Episodic memory, Event-related activation, fMRI, Sex, Voxel-based morphometry
National Category
Neurology
Identifiers
urn:nbn:se:uu:diva-305754 (URN)10.1016/j.bbr.2016.10.002 (DOI)000389086700038 ()27713000 (PubMedID)
Funder
Swedish Research Council, VR 2011-1943
Available from: 2016-10-21 Created: 2016-10-21 Last updated: 2018-04-17Bibliographically approved
2. Structural whole-brain covariance of the anterior and posterior hippocampus: Associations with age and memory
Open this publication in new window or tab >>Structural whole-brain covariance of the anterior and posterior hippocampus: Associations with age and memory
Show others...
2018 (English)In: Hippocampus, ISSN 1050-9631, E-ISSN 1098-1063, Vol. 28, no 2, p. 151-163Article in journal (Refereed) Published
Abstract [en]

The hippocampus (HC) interacts with distributed brain regions to support memory and shows significant volume reductions in aging, but little is known about age effects on hippocampal whole-brain structural covariance. It is also unclear whether the anterior and posterior HC show similar or distinct patterns of whole-brain covariance and to what extent these are related to memory functions organized along the hippocampal longitudinal axis. Using the multivariate approach partial least squares, we assessed structural whole-brain covariance of the HC in addition to regional volume, in young, middle-aged and older adults (n = 221), and assessed associations with episodic and spatial memory. Based on findings of sex differences in both memory and brain aging, we further considered sex as a potential modulating factor of age effects. There were two main covariance patterns: one capturing common anterior and posterior covariance, and one differentiating the two regions by capturing anterior-specific covariance only. These patterns were differentially related to associative memory while unrelated to measures of single-item memory and spatial memory. Although patterns were qualitatively comparable across age groups, participants' expression of both patterns decreased with age, independently of sex. The results suggest that the organization of hippocampal structural whole-brain covariance remains stable across age, but that the integrity of these networks decreases as the brain undergoes age-related alterations.

Place, publisher, year, edition, pages
John Wiley & Sons, 2018
Keywords
aging, episodic memory, longitudinal axis, sex, spatial memory
National Category
Neurology
Identifiers
urn:nbn:se:uu:diva-335505 (URN)10.1002/hipo.22817 (DOI)000422974700008 ()29171897 (PubMedID)
Funder
Swedish Research Council, 2009-2035Swedish Research Council, 2011-1943
Available from: 2017-12-06 Created: 2017-12-06 Last updated: 2019-06-28Bibliographically approved
3. Age-related hippocampal resting-state connectivity shows axis-dependent associations with memory
Open this publication in new window or tab >>Age-related hippocampal resting-state connectivity shows axis-dependent associations with memory
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Functional connectivity across large-scale brain networks alters in older age and changes are often associated with memory decline. Studies assessing hippocampal resting-state functional connectivity (rsFC), however, rarely consider the anterior and posterior hippocampus separately, although evidence suggests they are part of two distinct networks differentially supporting memory. While only a limited number of studies have considered age effects on axis-related hippocampal connectivity, findings suggest that rsFC of the two regions display differential effects of age. Reports on the link between such effects and memory are however inconclusive, and previous findings mainly concern episodic memory, ignoring spatial memory also dependent on the hippocampus. Here, we therefore assessed age effects on axis-related hippocampal rsFC, accounting for associations with both episodic and spatial memory in young, middle-aged and older adults (n=194). The anterior and posterior hippocampus showed different age-related decreases in connectivity assessed across middle and older age, but common to the regions was a decreased coupling with the medial orbitofrontal cortex. Only connectivity between the posterior hippocampus and the lingual gyrus increased as a function of age, displaying negative associations with episodic memory. In contrast, the region’s connectivity with the insula, decreasing with age, was positively related to spatial memory. Consistent with previous reports, our findings indicate that hippocampal rsFC vary with age in an axis-dependent manner, and further add to the knowledge on this differentiation’s relevance to memory by showing that age-related rsFC of the anterior and posterior hippocampus is differentially associated with episodic and spatial memory.

Keywords
Aging, Episodic Memory, Hippocampus, Longitudinal axis, Sex, Spatial Memory
National Category
Psychology
Identifiers
urn:nbn:se:uu:diva-348685 (URN)
Available from: 2018-04-17 Created: 2018-04-17 Last updated: 2018-04-17

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