Chronic stress increases prefrontal inhibition: a mechanism for stress-induced prefrontal dysfunction
Open accessAbstract
Background Multiple neuropsychiatric disorders, e.g., depression, are linked to imbalances in excitatory and inhibitory neurotransmission and prefrontal cortical dysfunction, and are concomitant with chronic stress.Methods We used electrophysiologic (n = 5-6 animals, 21-25 cells/group), neuroanatomic (n = 6-8/group), and behavioral (n = 12/group) techniques to test the hypothesis that chronic stress increases inhibition of medial prefrontal cortex (mPFC) glutamatergic output neurons.Results Using patch clamp recordings from infralimbic mPFC pyramidal neurons, we found that chronic stress selectively increases the frequency of miniature inhibitory postsynaptic currents with no effect on amplitude, which suggests that chronic stress increases presynaptic gamma-aminobutyric acid release. Elevated gamma-aminobutyric acid release under chronic stress is accompanied by increased inhibitory appositions and terminals onto glutamatergic cells, as assessed by both immunohistochemistry and electron microscopy. Furthermore, chronic stress decreases glucocorticoid receptor immunoreactivity specifically in a subset of inhibitory neurons, which suggests that increased inhibitory tone in the mPFC after chronic stress may be caused by loss of a glucocorticoid receptor-mediated brake on interneuron activity. These neuroanatomic and functional changes are associated with impairment of a prefrontal-mediated behavior. During chronic stress, rats initially make significantly more errors in the delayed spatial win-shift task, an mPFC-mediated behavior, which suggests a diminished impact of the mPFC on decision making.Conclusions Taken together, the data suggest that chronic stress increases synaptic inhibition onto prefrontal glutamatergic output neurons, limiting the influence of the prefrontal cortex in control of stress reactivity and behavior. Thus, these data provide a mechanistic link among chronic stress, prefrontal cortical hypofunction, and behavioral dysfunction.
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The infralimbic cortex is involved in coping with chronic stress, eventually leading to structural changes and prefrontal dysfunction.
“The most ventral subdomain of the mPFC is the infralimbic cortex (IL) and is involved in coping with chronic stress eventually leading to structural changes and prefrontal dysfunction [5–11].”
From Development of prefrontal cortex (2022) · cites this paper as [11]
Chronic stress is thought to have diffuse neurological consequences.
“The neurological sequelae of chronic stress is considered diffuse (33)”
From Neuroticism Traits Selectively Impact Long Term Illness Course and Cognitive Decline in Late-Life Depression (2017) · cites this paper as [33]
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Shepard, R., Page, C. E., & Coutellier, L. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.06.038 · Cited by 118 · see citing works
Shepard, R., & Coutellier, L. (2018) · Molecular Neurobiology · doi:10.1007/s12035-017-0528-0 · Cited by 97 · see citing works
Ghosal, S., Duman, C. H., Liu, R.-J., Wu, M., Terwilliger, R., Girgenti, M. J., Wohleb, E., Fogaca, M. V., Teichman, E. M., Hare, B., et al. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104669 · Cited by 89 · see citing works
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Abnormal stress responsiveness and suicidal behavior: a risk phenotype
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Self-citation
- Authors
- McKlveen, J. M., Morano, R. L., Fitzgerald, M., Zoubovsky, S., Cassella, S. N., Scheimann, J. R., Ghosal, S., Mahbod, P., Packard, B. A., Myers, B., Baccei, M. L., & Herman, J. P.
- Affiliations
- University of Cincinnati (US)
- Corresponding author
- Herman, James P.
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2016-11
- Volume
- 80
- Issue
- 10
- Pages
- 754-764
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC5629635
- OpenAlex
- W2323003929
- Cited by
- 224
- References
- 95
- Citations by year
- 2026: 16 · 2025: 27 · 2024: 25 · 2023: 13 · 2022: 27 · 2021: 26 · 2020: 23 · 2019: 25 · 2018: 24 · 2017: 10 · 2016: 8
- FWCI
- 14.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (MH097430, MH069860, MH049698, HL122454)
- American Heart Association (17070152)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- chronic stress, medial prefrontal cortex, infralimbic cortex, GABAergic inhibition, presynaptic GABA release, inhibitory postsynaptic currents, glucocorticoid receptor, interneurons, decision-making, stress reactivity, depression, excitation-inhibition balance
- MeSH terms
- Animals, Behavior, Animal, Chronic Disease, Disease Models, Animal, gamma-Aminobutyric Acid, Male, Neural Inhibition, Receptors, Glucocorticoid, Rats, Sprague-Dawley, Prefrontal Cortex, Pyramidal Cells, Patch-Clamp Techniques, Glutamic Acid, Rats, Inhibitory Postsynaptic Potentials
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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