Stress Impairs Prefrontal Cortical Function via D1 Dopamine Receptor Interactions With Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
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Background Psychiatric disorders such as schizophrenia are worsened by stress, and working memory deficits are often a central feature of illness. Working memory is mediated by the persistent firing of prefrontal cortical (PFC) pyramidal neurons. Stress impairs working memory via high levels of dopamine D1 receptor (D1R) activation of cyclic adenosine monophosphate signaling, which reduces PFC neuronal firing. The current study examined whether D1R-cyclic adenosine monophosphate signaling reduces neuronal firing and impairs working memory by increasing the open state of hyperpolarization-activated cyclic nucleotide-gated (HCN) cation channels, which are concentrated on dendritic spines where PFC pyramidal neurons interconnect.Methods A variety of methods were employed to test this hypothesis: dual immunoelectron microscopy localized D1R and HCN channels, in vitro recordings tested for D1R actions on HCN channel current, while recordings in monkeys performing a working memory task tested for D1R-HCN channel interactions in vivo. Finally, cognitive assessments following intra-PFC infusions of drugs examined D1R-HCN channel interactions on working memory performance.Results Immunoelectron microscopy confirmed D1R colocalization with HCN channels near excitatory-like synapses on dendritic spines in primate PFC. Mouse PFC slice recordings demonstrated that D1R stimulation increased HCN channel current, while local HCN channel blockade in primate PFC protected task-related firing from D1R-mediated suppression. D1R stimulation in rat or monkey PFC impaired working memory performance, while HCN channel blockade in PFC prevented this impairment in rats exposed to either stress or D1R stimulation.Conclusions These findings suggest that D1R stimulation or stress weakens PFC function via opening of HCN channels at network synapses.
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Inhibition of Ca2+-PKC or cAMP-PKA signaling, or blockade of HCN channels, can rescue PFC delay-cell firing and working memory functions.
“Conversely, inhibition of Ca2+–PKC or cAMP–PKA signaling, or blockade of HCN channels, can rescue PFC delay-cell firing and working memory functions57,60,62.”
From Stress weakens prefrontal networks: molecular insults to higher cognition (2015) · cites this paper as [62]
High levels of D1R activation of cAMP signaling reduces PFC neuronal firing and impairs working memory via opening of HCN channels at excitatory synapses.
“High levels of D1R activation of cAMP signaling reduces PFC neuronal firing and impairs working memory via opening of HCN channels at excitatory synapses 54.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [54]
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- Authors
- Gamo, N. J., Lur, G., Higley, M. J., Wang, M., Paspalas, C. D., Vijayraghavan, S., Yang, Y., Ramos, B. P., Peng, K., Kata, A., Boven, L., Lin, F., Roman, L., Lee, D., & Arnsten, A. F. T.
- Affiliations
- Yale University (US)
- Corresponding author
- Gamo, Nao J.
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2015-12
- Volume
- 78
- Issue
- 12
- Pages
- 860-870
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC4524795
- OpenAlex
- W2002940328
- Cited by
- 97
- References
- 87
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 6 · 2023: 10 · 2022: 18 · 2021: 8 · 2020: 3 · 2019: 9 · 2018: 7 · 2017: 11 · 2016: 9 · 2015: 5 · 2014: 1
- FWCI
- 4.98
- 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)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Yale University
- National Alliance for Research on Schizophrenia and Depression
- National Institute on Alcohol Abuse and Alcoholism (RL1AA017536)
- National Institute of Mental Health (MH099045, R01MH099045)
- National Institute of Neurological Disorders and Stroke (NS-07224, T32NS007224)
- National Center for Research Resources (U54RR024350)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- stress, dopamine D1 receptor, HCN channels, prefrontal cortex, working memory, neuronal firing, dendritic spines, synaptic transmission, cAMP signaling, schizophrenia
- MeSH terms
- Action Potentials, Animals, Macaca mulatta, Male, Memory, Short-Term, Pyrimidines, Stress, Physiological, Synapses, 2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine, Rats, Sprague-Dawley, Prefrontal Cortex, Receptors, Dopamine D1, Pyramidal Cells, Dendritic Spines, Mice, Rats, Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
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.
Statistics and arithmetic are recomputed, not judged.
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