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Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress
Open accessAbstract
The prefrontal cortex r regulates behavior, cognition, and emotion by using working memory. Prefrontal functions are impaired by stress exposure. Acute, stress-induced deficits arise from excessive protein kinase C (PKC) signaling, which diminishes prefrontal neuronal firing. Chronic stress additionally produces architectural changes, reducing dendritic complexity and spine density of cortico-cortical pyramidal neurons, thereby disrupting excitatory working memory networks. In vitro studies have found that sustained PKC activity leads to spine loss from hippocampal-cultured neurons, suggesting that PKC may contribute to spine loss during chronic stress exposure. The present study tested whether inhibition of PKC with chelerythrine before daily stress would protect prefrontal spines and working memory. We found that inhibition of PKC rescued working memory impairments and reversed distal apical dendritic spine loss in layer II/III pyramidal neurons of rat prelimbic cortex. Greater spine density predicted better cognitive performance, the first direct correlation between pyramidal cell structure and working memory abilities. These findings suggest that PKC inhibitors may be neuroprotective in disorders with dysregulated PKC signaling such as bipolar disorder, schizophrenia, post-traumatic stress disorder, and lead poisoning—conditions characterized by impoverished prefrontal structural and functional integrity.
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“Chronic exposure to uncontrollable stress causes loss of spines and dendrites in the prefrontal cortex (PFC), a recently evolved brain region that provides top-down regulation of thought, action, and emotion.”
From Chronic Stress Weakens Connectivity in the Prefrontal Cortex: Architectural and Molecular Changes. (2021) · cites this paper as [16]
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“stress increases, while guanfacine inhibits, the feedforward Ca2+-cAMP-PKA-K+ actions that weaken PFC network connectivity, neuronal firing and function.”
From Guanfacine’s mechanism of action in treating prefrontal cortical disorders: Successful translation across species (2020) · cites this paper as Hains et al., 2009
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“stress increases, while guanfacine inhibits, the feedforward Ca2+-cAMP-PKA-K+ actions that weaken PFC network connectivity, neuronal firing and function.”
From Guanfacine’s mechanism of action in treating prefrontal cortical disorders: Successful translation across species (2020) · cites this paper as Hains et al., 2009
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“Loss of dendritic spines and/or dendrites is accompanied by, and often correlates with, the loss of PFC cognitive functioning.”
From Chronic Stress Weakens Connectivity in the Prefrontal Cortex: Architectural and Molecular Changes. (2021) · cites this paper as [16]
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“With chronic stress exposure, dendritic spines are lost from layer II/III pyramidal cells in rat mPFC”
From Guanfacine’s mechanism of action in treating prefrontal cortical disorders: Successful translation across species (2020) · cites this paper as Hains et al., 2009
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“Research in rats by Avis Hains has shown that inhibition of PKC or PKA signaling can prevent the loss of mPFC dendritic spines and working memory abilities during chronic stress exposure (Hains et al., 2009, Hains et al., 2015), suggesting that the sustained weakening of synaptic connectivity via K+ channel opening contributes to spine loss.”
From Guanfacine’s mechanism of action in treating prefrontal cortical disorders: Successful translation across species (2020) · cites this paper as Hains et al., 2009
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“With chronic stress exposure, there is architectural loss of mPFC spines and dendrites (Moda-Sava et al., 2019, Radley et al., 2006) that correlates with impaired PFC cognitive functioning (Hains et al., 2009, Hains et al., 2015, Liston et al., 2006).”
From Guanfacine’s mechanism of action in treating prefrontal cortical disorders: Successful translation across species (2020) · cites this paper as Hains et al., 2009
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“Dendritic spine loss from layer II/III pyramidal cells in the prelimbic medial PFC correlates with impaired working memory on the delayed alternation task75.”
From Stress weakens prefrontal networks: molecular insults to higher cognition (2015) · cites this paper as [75]
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“The protection of dendritic spines correlates with preserved working memory function75.”
From Stress weakens prefrontal networks: molecular insults to higher cognition (2015) · cites this paper as [75]
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“Inhibition of PKC signaling before daily stress exposure in rats prevents the loss of spines from layer II/III PFC pyramidal cells normally observed with chronic stress75.”
From Stress weakens prefrontal networks: molecular insults to higher cognition (2015) · cites this paper as [75]
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Metadata
- Authors
- Hains, A. B., Vu, M. A. T., Maciejewski, P. K., van Dyck, C. H., Gottron, M., & Arnsten, A. F. T.
- Affiliations
- Yale University (US)
- Corresponding author
- Arnsten, Amy F. T.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-10-20
- Volume
- 106
- Issue
- 42
- Pages
- 17957-17962
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2742406
- OpenAlex
- W1996838710
- Cited by
- 234
- References
- 66
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 7 · 2023: 12 · 2022: 15 · 2021: 23 · 2020: 13 · 2019: 15 · 2018: 13 · 2017: 19 · 2016: 14 · 2015: 20 · 2014: 15 · 2013: 17 · 2012: 12
- FWCI
- 5.82
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- U.S. Public Health Service
- National Institute on Alcohol Abuse and Alcoholism (RL1AA017536)
- National Institute on Aging (R37AG006036)
- National Institute of Mental Health (P50MH068789)
- National Institute of Neurological Disorders and Stroke (K25NS044316)
- National Center for Research Resources (U54RR024350)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- protein kinase C, chronic stress, dendritic spines, prefrontal cortex, working memory, chelerythrine, prelimbic cortex, pyramidal neurons, spine loss, neuroprotection, cognitive impairment, bipolar disorder, schizophrenia, post-traumatic stress disorder, lead poisoning
- MeSH terms
- Animals, Atrophy, Cognition, Disease Models, Animal, Humans, Male, Memory, Models, Neurological, Protein Kinase C, Stress, Physiological, Stress, Psychological, Signal Transduction, Rats, Sprague-Dawley, Prefrontal Cortex, Protein Kinase Inhibitors, Dendritic Spines, Rats, Benzophenanthridines
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