Amyloid-β oligomers in the nucleus accumbens decrease motivation via insertion of calcium-permeable AMPA receptors

It is essential to identify the neuronal mechanisms of Alzheimer’s Disease (AD)-associated neuropsychiatric symptoms, e.g., apathy, before improving the life quality of AD patients. Here, we focused on the nucleus accumbens (NAc), a critical brain region processing motivation, also known to display...

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Published inMolecular psychiatry Vol. 27; no. 4; pp. 2146 - 2157
Main Authors Guo, Changyong, Wen, Di, Zhang, Yihong, Mustaklem, Richie, Mustaklem, Basil, Zhou, Miou, Ma, Tao, Ma, Yao-Ying
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.04.2022
Nature Publishing Group
Subjects
14/19
14/32
14/34
631/337
631/378
64/60
692/699/476/1414
9/74
alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid
Alzheimer Disease - pathology
Alzheimer's disease
Amyloid beta-Peptides - metabolism
Behavioral Sciences
Biological Psychology
Calcium - metabolism
Calcium permeability
Emotional behavior
Humans
Medicine
Medicine & Public Health
Mental disorders
Motivation
Neurodegeneration
Neurodegenerative diseases
Neurosciences
Nucleus accumbens
Nucleus Accumbens - metabolism
Oligomers
Pharmacotherapy
Psychiatry
Quality of life
Receptors, AMPA - metabolism
Receptors, Calcium-Sensing
Synapses - metabolism
Synaptic transmission
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
β-Amyloid
Online AccessGet full text

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Abstract It is essential to identify the neuronal mechanisms of Alzheimer’s Disease (AD)-associated neuropsychiatric symptoms, e.g., apathy, before improving the life quality of AD patients. Here, we focused on the nucleus accumbens (NAc), a critical brain region processing motivation, also known to display AD-associated pathological changes in human cases. We found that the synaptic calcium permeable (CP)-AMPA receptors (AMPARs), which are normally absent in the NAc, can be revealed by acute exposure to Aβ oligomers (AβOs), and play a critical role in the emergence of synaptic loss and motivation deficits. Blockade of NAc CP-AMPARs can effectively prevent AβO-induced downsizing and pruning of spines and silencing of excitatory synaptic transmission. We conclude that AβO-triggered synaptic insertion of CP-AMPARs is a key mechanism mediating synaptic degeneration in AD, and preserving synaptic integrity may prevent or delay the onset of AD-associated psychiatric symptoms.
AbstractList It is essential to identify the neuronal mechanisms of Alzheimer's Disease (AD)-associated neuropsychiatric symptoms, e.g., apathy, before improving the life quality of AD patients. Here, we focused on the nucleus accumbens (NAc), a critical brain region processing motivation, also known to display AD-associated pathological changes in human cases. We found that the synaptic calcium permeable (CP)-AMPA receptors (AMPARs), which are normally absent in the NAc, can be revealed by acute exposure to Aβ oligomers (AβOs), and play a critical role in the emergence of synaptic loss and motivation deficits. Blockade of NAc CP-AMPARs can effectively prevent AβO-induced downsizing and pruning of spines and silencing of excitatory synaptic transmission. We conclude that AβO-triggered synaptic insertion of CP-AMPARs is a key mechanism mediating synaptic degeneration in AD, and preserving synaptic integrity may prevent or delay the onset of AD-associated psychiatric symptoms.
It is essential to identify the neuronal mechanisms of Alzheimer’s Disease (AD)-associated neuropsychiatric symptoms, e.g., apathy, before improving the life quality of AD patients. Here, we focused on the nucleus accumbens (NAc), a critical brain region processing motivation, also known to display AD-associated pathological changes in human cases. We found that the synaptic calcium permeable (CP)-AMPA receptors (AMPARs), which are normally absent in the NAc, can be revealed by acute exposure to Aβ oligomers (AβOs), and play a critical role in the emergence of synaptic loss and motivation deficits. Blockade of NAc CP-AMPARs can effectively prevent AβO-induced downsizing and pruning of spines and silencing of excitatory synaptic transmission. We conclude that AβO-triggered synaptic insertion of CP-AMPARs is a key mechanism mediating synaptic degeneration in AD, and preserving synaptic integrity may prevent or delay the onset of AD-associated psychiatric symptoms. Amyloid-β oligomers in the nucleus accumbens lead to excitatory synapse loss and reduced motivation due to activation of calcium-permeable AMPA receptors.
Author Ma, Yao-Ying
Wen, Di
Mustaklem, Richie
Mustaklem, Basil
Ma, Tao
Zhang, Yihong
Zhou, Miou
Guo, Changyong
AuthorAffiliation 5 Lead Contact
3 Department of Internal Medicine-Gerontology and Geriatric Medicine; Department of Physiology and Pharmacology; Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC 27101, USA
2 Graduate College of Biomedical Sciences, Western University of Health Sciences, Pomona, CA 91766, USA
1 Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN 46202, USA
4 Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN 46202, USA
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– name: 4 Stark Neurosciences Research Institute, Indiana University School of Medicine, Indianapolis, IN 46202, USA
– name: 3 Department of Internal Medicine-Gerontology and Geriatric Medicine; Department of Physiology and Pharmacology; Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC 27101, USA
– name: 2 Graduate College of Biomedical Sciences, Western University of Health Sciences, Pomona, CA 91766, USA
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Notes Experimental design: CG, MZ, TM, YM. Data collection: CG, DW, YZ, RM, BM, YM. Data analysis: CG, DW, YZ, YM. Paper writing: CG, DW, TM, YM.
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Snippet It is essential to identify the neuronal mechanisms of Alzheimer’s Disease (AD)-associated neuropsychiatric symptoms, e.g., apathy, before improving the life...
It is essential to identify the neuronal mechanisms of Alzheimer's Disease (AD)-associated neuropsychiatric symptoms, e.g., apathy, before improving the life...
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StartPage 2146
SubjectTerms 14/19
14/32
14/34
631/337
631/378
64/60
692/699/476/1414
9/74
alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid
Alzheimer Disease - pathology
Alzheimer's disease
Amyloid beta-Peptides - metabolism
Behavioral Sciences
Biological Psychology
Calcium - metabolism
Calcium permeability
Emotional behavior
Humans
Medicine
Medicine & Public Health
Mental disorders
Motivation
Neurodegeneration
Neurodegenerative diseases
Neurosciences
Nucleus accumbens
Nucleus Accumbens - metabolism
Oligomers
Pharmacotherapy
Psychiatry
Quality of life
Receptors, AMPA - metabolism
Receptors, Calcium-Sensing
Synapses - metabolism
Synaptic transmission
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
β-Amyloid
Title Amyloid-β oligomers in the nucleus accumbens decrease motivation via insertion of calcium-permeable AMPA receptors
URI https://link.springer.com/article/10.1038/s41380-022-01459-0
https://www.ncbi.nlm.nih.gov/pubmed/35105968
https://www.proquest.com/docview/2667959137
https://pubmed.ncbi.nlm.nih.gov/PMC9133055
Volume 27
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