Cerebellar-limbic neurocircuit is the novel biosignature of physiocognitive decline syndrome

Li Kuo Liu; Kun Hsien Chou; Chih Chin Heather Hsu; Li Ning Peng; Wei Ju Lee; Wei Ta Chen; Ching Po Lin; Chih Ping Chung; Pei Ning Wang; Liang Kung Chen

doi:10.18632/aging.104135

Cerebellar-limbic neurocircuit is the novel biosignature of physiocognitive decline syndrome

Li Kuo Liu, Kun Hsien Chou, Chih Chin Heather Hsu, Li Ning Peng, Wei Ju Lee, Wei Ta Chen, Ching Po Lin, Chih Ping Chung^*, Pei Ning Wang, Liang Kung Chen

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

37 Scopus citations

Abstract

Both physical and cognitive deficits occur in the aging process. We operationally defined the phenomenon as physio-cognitive decline syndrome (PCDS) and aimed to decipher its corresponding neuroanatomy patterns and neurocircuit. High resolution 3T brain magnetic resonance imaging (MRI) images from a community-dwelling longitudinal aging cohort were analysed. PCDS was defined as weakness (handgrip strength) and/or slowness (gait speed) concomitant with impairment in any cognitive domain (defined by 1.5 standard deviation below age, sex-matched norms), but without dementia or disability. Among 1196 eligible ≥ 50-year-old (62±9 years, 47.6%men) subjects, 15.9% had PCDS. Compared to the other participants, individuals with PCDS had significantly lower gray-matter volume (GMV) in the bilateral amygdala and thalamus, right hippocampus, right temporo-occipital cortex, and left cerebellum VI and V regions. The regions of reduced GMV in people with PCDS were similar between the middle-aged and older adults; whereas larger clusters with more extensive GMV-depleted regions were observed in ≥65-year-olds with PCDS. Diffusion-weighted tractography showed disrupted hippocampus-amygdala-cerebellum connections in subjects with PCDS. The neuroanatomic characteristics revealed by this study provide evidence for pathophysiological processes associated with concomitant physio-cognitive decline in the elderly. This neurocircuit might constitute a target for future preventive interventions.

Original language	English
Pages (from-to)	25319-25336
Number of pages	18
Journal	Aging
Volume	12
Issue number	24
DOIs	https://doi.org/10.18632/aging.104135
State	Published - 31 Dec 2020

Keywords

brain volume
cognitive impairment
diffusion-weighted tractography
frailty
magnetic resonance imaging

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title = "Cerebellar-limbic neurocircuit is the novel biosignature of physiocognitive decline syndrome",

abstract = "Both physical and cognitive deficits occur in the aging process. We operationally defined the phenomenon as physio-cognitive decline syndrome (PCDS) and aimed to decipher its corresponding neuroanatomy patterns and neurocircuit. High resolution 3T brain magnetic resonance imaging (MRI) images from a community-dwelling longitudinal aging cohort were analysed. PCDS was defined as weakness (handgrip strength) and/or slowness (gait speed) concomitant with impairment in any cognitive domain (defined by 1.5 standard deviation below age, sex-matched norms), but without dementia or disability. Among 1196 eligible ≥ 50-year-old (62±9 years, 47.6%men) subjects, 15.9% had PCDS. Compared to the other participants, individuals with PCDS had significantly lower gray-matter volume (GMV) in the bilateral amygdala and thalamus, right hippocampus, right temporo-occipital cortex, and left cerebellum VI and V regions. The regions of reduced GMV in people with PCDS were similar between the middle-aged and older adults; whereas larger clusters with more extensive GMV-depleted regions were observed in ≥65-year-olds with PCDS. Diffusion-weighted tractography showed disrupted hippocampus-amygdala-cerebellum connections in subjects with PCDS. The neuroanatomic characteristics revealed by this study provide evidence for pathophysiological processes associated with concomitant physio-cognitive decline in the elderly. This neurocircuit might constitute a target for future preventive interventions.",

keywords = "brain volume, cognitive impairment, diffusion-weighted tractography, frailty, magnetic resonance imaging",

author = "Liu, {Li Kuo} and Chou, {Kun Hsien} and {Heather Hsu}, {Chih Chin} and Peng, {Li Ning} and Lee, {Wei Ju} and Chen, {Wei Ta} and Lin, {Ching Po} and Chung, {Chih Ping} and Wang, {Pei Ning} and Chen, {Liang Kung}",

note = "Publisher Copyright: {\textcopyright} 2020. Liu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. All Rights Reserved.",

year = "2020",

month = dec,

day = "31",

doi = "10.18632/aging.104135",

language = "English",

volume = "12",

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journal = "Aging",

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T1 - Cerebellar-limbic neurocircuit is the novel biosignature of physiocognitive decline syndrome

AU - Liu, Li Kuo

AU - Chou, Kun Hsien

AU - Heather Hsu, Chih Chin

AU - Peng, Li Ning

AU - Lee, Wei Ju

AU - Chen, Wei Ta

AU - Lin, Ching Po

AU - Chung, Chih Ping

AU - Wang, Pei Ning

AU - Chen, Liang Kung

N1 - Publisher Copyright: © 2020. Liu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. All Rights Reserved.

PY - 2020/12/31

Y1 - 2020/12/31

N2 - Both physical and cognitive deficits occur in the aging process. We operationally defined the phenomenon as physio-cognitive decline syndrome (PCDS) and aimed to decipher its corresponding neuroanatomy patterns and neurocircuit. High resolution 3T brain magnetic resonance imaging (MRI) images from a community-dwelling longitudinal aging cohort were analysed. PCDS was defined as weakness (handgrip strength) and/or slowness (gait speed) concomitant with impairment in any cognitive domain (defined by 1.5 standard deviation below age, sex-matched norms), but without dementia or disability. Among 1196 eligible ≥ 50-year-old (62±9 years, 47.6%men) subjects, 15.9% had PCDS. Compared to the other participants, individuals with PCDS had significantly lower gray-matter volume (GMV) in the bilateral amygdala and thalamus, right hippocampus, right temporo-occipital cortex, and left cerebellum VI and V regions. The regions of reduced GMV in people with PCDS were similar between the middle-aged and older adults; whereas larger clusters with more extensive GMV-depleted regions were observed in ≥65-year-olds with PCDS. Diffusion-weighted tractography showed disrupted hippocampus-amygdala-cerebellum connections in subjects with PCDS. The neuroanatomic characteristics revealed by this study provide evidence for pathophysiological processes associated with concomitant physio-cognitive decline in the elderly. This neurocircuit might constitute a target for future preventive interventions.

AB - Both physical and cognitive deficits occur in the aging process. We operationally defined the phenomenon as physio-cognitive decline syndrome (PCDS) and aimed to decipher its corresponding neuroanatomy patterns and neurocircuit. High resolution 3T brain magnetic resonance imaging (MRI) images from a community-dwelling longitudinal aging cohort were analysed. PCDS was defined as weakness (handgrip strength) and/or slowness (gait speed) concomitant with impairment in any cognitive domain (defined by 1.5 standard deviation below age, sex-matched norms), but without dementia or disability. Among 1196 eligible ≥ 50-year-old (62±9 years, 47.6%men) subjects, 15.9% had PCDS. Compared to the other participants, individuals with PCDS had significantly lower gray-matter volume (GMV) in the bilateral amygdala and thalamus, right hippocampus, right temporo-occipital cortex, and left cerebellum VI and V regions. The regions of reduced GMV in people with PCDS were similar between the middle-aged and older adults; whereas larger clusters with more extensive GMV-depleted regions were observed in ≥65-year-olds with PCDS. Diffusion-weighted tractography showed disrupted hippocampus-amygdala-cerebellum connections in subjects with PCDS. The neuroanatomic characteristics revealed by this study provide evidence for pathophysiological processes associated with concomitant physio-cognitive decline in the elderly. This neurocircuit might constitute a target for future preventive interventions.

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KW - cognitive impairment

KW - diffusion-weighted tractography

KW - frailty

KW - magnetic resonance imaging

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VL - 12

SP - 25319

EP - 25336

JO - Aging

JF - Aging

IS - 24

ER -

Cerebellar-limbic neurocircuit is the novel biosignature of physiocognitive decline syndrome

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