Heritability of hippocampal functional and microstructural organisation

Bayrak, Şeyma; Wael, Reinder Vos de; Schaare, H. Lina; Hettwer, Meike D.; Caldairou, Benoît; Bernasconi, Andrea; Bernasconi, Neda; Bernhardt, Boris C.; Valk, Sofie L.

doi:10.1016/j.neuroimage.2022.119656

Cited by 15 publications

(15 citation statements)

References 124 publications

(215 reference statements)

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“…As expected, we found marked sex-differences that differed as a function of hippocampal subfield, with subiculum showing higher T1wT2w values in females, but CA2/3 showing higher T1wT2w mean in males relative to females. Though research on sex differences in hippocampal structure in humans mainly focuses on the whole hippocampal volume, recent work has indicated marked changes in particular in subicular microstructure (Bayrak et al, 2022) and volume (van Eijk et al, 2020). Previous work in rats has shown marked changes in CA1 and CA3 but not CA2 (Yagi et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Relating sex differences in cortical and hippocampal microstructure to sex hormones

Küchenhoff,

Bayrak,

Zsido

et al. 2023

Preprint

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Sex hormone receptors are expressed widely in both neurons and glial cells, which allows them to interact with the brain’s major cell groups via several molecular mechanisms. These mechanisms lead to sex differences in brain structure as well as hormone-induced plasticity in the female brain across the menstrual cycle. Adding to the literature on volumetric changes in cortical structure, here we set out to investigate sex differences in the microstructure of the human cortex in relation to sex hormones. We assessed regional variation in cortical microstructure as a function of sex, hormonal status and sex hormone receptor gene expression distribution based on quantitative intracortical profilingin vivousing the magnetic resonance imaging based T1w/T2w ratio in 992 healthy females and males of the Human Connectome Project young adult sample. We demonstrate that microstructure in isocortex and hippocampus differs regionally between males and females, that this effect varies with hormone levels of females and that implicated brain regions overlap with estrogen receptor and sex steroid synthesis gene expression. Lastly, we show that sex and sex hormone related brain structure variations are most pronounced in areas of low laminar cortical complexity (agranular cortex), which are also predicted to be most plastic based on their cytoarchitectural properties. Together, our data thus are suggestive of sex differences in cortical and hippocampal microstructure, as well as the modulatory function of sex hormones on these measures. Albeit correlative, this study underscores the importance of incorporating sex hormone variables into the investigation of brain structure and plasticity.

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Section: Discussionmentioning

confidence: 99%

Relating sex differences in cortical and hippocampal microstructure to sex hormones

Küchenhoff,

Bayrak,

Zsido

et al. 2023

Preprint

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“…In previous validations, this algorithm has shown high segmentation accuracy of hippocampal subfields (72), and in detecting hippocampal subfield pathology in patients with epilepsy (113). It was furthermore demonstrated that these representations can be used to probe sub-regional functional organization of the hippocampus (33, 34). Hippocampal volumes were estimated based on T1w data that were linearly registered to MNI152, such that intracranial volume was implicitly controlled for.…”

Section: Methodsmentioning

confidence: 99%

“…These subfields have unique microstructure (22)(23)(24)(25)(26) and participate differently in the hippocampal circuitry (27), likely implicating different functions (28)(29)(30)(31)(32)(33). Indeed, intrinsic functional MRI analyses during wakeful rest have shown that the hippocampal subfields show functional signal correlations with a broad range of cortical regions, part of visual, control, and default functional networks (26,(33)(34)(35)(36). Hippocampal subfield volumes and associated intrinsic functional connectivity have been shown to be heritable (34,37), indicating that individual variation in subfield structure and function is, in part, under genetic control.…”

Section: Introductionmentioning

confidence: 99%

“…Indeed, intrinsic functional MRI analyses during wakeful rest have shown that the hippocampal subfields show functional signal correlations with a broad range of cortical regions, part of visual, control, and default functional networks (26,(33)(34)(35)(36). Hippocampal subfield volumes and associated intrinsic functional connectivity have been shown to be heritable (34,37), indicating that individual variation in subfield structure and function is, in part, under genetic control. Other lines of research have reported hippocampal structure and function to be highly sensitive to contextual factors such as stress (21).…”

Section: Introductionmentioning

confidence: 99%

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Differential increase of hippocampal subfield volume after socio-affective mental training relates to reductions in diurnal cortisol

Valk

Engert

Puhlmann

et al. 2023

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The hippocampus forms a central modulator of the HPA-axis, impacting the regulation of stress on brain structure, function, and behavior. The current study assessed whether three different types of 3-months mental training modules geared towards nurturing a) attention-based mindfulness, b) socio-affective skills, or c) socio-cognitive abilities may impact hippocampal integrity by reducing stress. We evaluated mental training-induced changes in hippocampal subfield volume and intrinsic functional connectivity, based on resting-state fMRI connectivity analysis in a group of healthy adults (N=332). We then related these changes to changes in diurnal and chronic cortisol levels. We observed increases in bilateral cornu ammonis volume (CA1-3) following the 3-months compassion-based module targeting socio-affective skills (Affect module), as compared to socio-cognitive skills (Perspective module) or a waitlist cohort that did not undergo an intervention. Structural changes were paralleled by increases in functional connectivity of CA1-3 when fostering socio-affective as compared to socio-cognitive skills. Moreover, training-related changes in CA1-3 structure and function consistently correlated with reduction in cortisol output. In sum, we provide a link between socio-emotional behavioral intervention, CA1-3 structure and function, and cortisol reductions in healthy adults.

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“…Such differentiation is reflected in its microstructure, gross morphology, connectivity, gene expression, electrophysiological properties, representational granularity, and functional profiles. This anterior-posterior distinction is not characterized by abrupt shifts but rather by a continuous spectrum or gradient that extends along the long-axis, encompassing multiple organizational traits 2,4–6,25,26 . Consequently, investigating the gradient along the long-axis aids in comprehending how the hippocampus processes information and facilitates diverse cognitive functions, along with revealing its implications for various neurological and psychiatric conditions 1,3,24 .…”

mentioning

confidence: 99%

Dual long-axis reorganization of hippocampus in youth

Zeng,

Li,

et al. 2023

Preprint

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The reorganization of human hippocampus, especially its interaction with cortex, remains largely undefined in youth. The organization of a single hippocampal long-axis has been predominantly characterized as monotonic1–6, despite recent indications of nonmonotonic features in neuron density7and geometric eigenmodes8. While the human cortical hierarchy has been well recognized for significant developmental and evolutionary advantages9–12, hippocampus has been typically considered an evolutionarily conserved brain structure1,13,14, and overlooked regarding its integrative role of cortical hierarchical processing during development. Here, we corroborated the presence and significance of a dual long-axis representation of the hippocampal connectome and geometry including both linear and quadratic gradients along its long-axis in youth. This finding was robust across two independent large-scale developmental cohorts. Charting development of the dual long-axis gradients underscored their specific contributions to the cortical hierarchy maturation from the frontoparietal and salience/ventral attention networks. The observed developmental variability in spontaneous brain activities in youth parallels the gradients of myelin content. During childhood through adolescence to early adulthood, the hippocampus reorganized the dual long-axis by gradually relaxing its geometric constraints on the intrinsic network organization of cortical spontaneous activity for refined executive functions. Molecular processes underlying such reorganization of the dual long-axis in hippocampus are linked to neural growth, stress hormone regulation, and neuroactive signaling. Our findings enrich the understanding of hippocampal-cortical reorganizational principles across structural, functional, and molecular dimensions as well as its maturation, and define the plasticity distribution within the human hippocampus at systems level, holding potentials to enhance and translate neurodevelopment and neuropsychiatric healthcare.

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Heritability of hippocampal functional and microstructural organisation

Cited by 15 publications

References 124 publications

Relating sex differences in cortical and hippocampal microstructure to sex hormones

Relating sex differences in cortical and hippocampal microstructure to sex hormones

Differential increase of hippocampal subfield volume after socio-affective mental training relates to reductions in diurnal cortisol

Dual long-axis reorganization of hippocampus in youth

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