Fast oscillatory activity in the anterior cingulate cortex: dopaminergic modulation and effect of perineuronal net loss
Open accessAbstract
Dopamine release in the prefrontal cortex plays a critical role in cognitive function such as working memory, attention and planning. Dopamine exerts complex modulation on excitability of pyramidal neurons and interneurons, and regulates excitatory and inhibitory synaptic transmission. Because of the complexity of this modulation, it is difficult to fully comprehend the effect of dopamine on neuronal network activity. In this study, we investigated the effect of dopamine on local high-frequency oscillatory neuronal activity (in β band) in slices of the mouse anterior cingulate cortex (ACC). We found that dopamine enhanced the power of these oscillations induced by kainate and carbachol, but did not affect their peak frequency. Activation of D2R and in a lesser degree D1R increased the oscillation power, while activation of D4R had no effect. These high-frequency oscillations in the ACC relied on both phasic inhibitory and excitatory transmission and functional gap junctions. Thus, dopamine released in the ACC promotes high-frequency synchronized local cortical activity which is known to favor information transfer, fast selection and binding of distributed neuronal responses. Finally, the power of these oscillations was significantly enhanced after degradation of the perineuronal nets (PNNs) enwrapping most parvalbumin interneurons. This study provides new insights for a better understanding of the abnormal prefrontal gamma activity in schizophrenia (SZ) patients who display prefrontal anomalies of both the dopaminergic system and the PNNs.
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Ethanol, nicotine, cocaine, and heroin alter the intensity or number of PNNs in various brain regions.
“Several classes of drugs, including ethanol, nicotine, cocaine, and heroin, alter the intensity or number of PNNs in various brain regions, including the mPFC [154, 155], anterior cingulate cortex [131], orbitofrontal cortex [156], barrel cortex [157], insula [158], hypothalamus [159, 160], ventral tegmental area [156], and cerebellum [161–164].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [131]
The Results section (Figure 5; page unavailable) reports that chondroitinase ABC injection degraded PNNs in the anterior cingulate cortex. It does not report that ethanol, nicotine, cocaine, or heroin altered PNN intensity or number; the reported intervention was an enzyme injection. (LLM, conf=0.81)
Experimental — accuracy not yet measuredAll social memory associated regions are highly populated with PNN-surrounded PV neurons.
“All the social memory associated regions are highly populated with PNN-surrounded PV neurons [46, 66, 130, 131].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [131]
The Results section (page unavailable) says that most mature parvalbumin interneurons are surrounded by PNNs and documents PNNs around these cells in the anterior cingulate cortex. It does not establish that all social-memory-associated regions are highly populated with such neurons, or identify those regions as a group. (LLM, conf=0.85)
Experimental — accuracy not yet measuredNetwork oscillatory activity that was increased by drug-induced changes in dopaminergic signaling in mouse prefrontal cortex was further enhanced following chABC-mediated degradation of PNNs.
“For example, network oscillatory activity that was increased by drug-induced changes in dopaminergic signaling in mouse prefrontal cortex was further enhanced following chABC-mediated degradation of PNNs (Steullet et al., 2014).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Steullet et al., 2014
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References 78 · Cited by 49
Research works printed but not linked: 2
- Chan R. C. Di X. McAlonan G. M. Gong Q. Y. (2011). Brain anatomical abnormalities in high-risk individuals, first-episode and chronic schizophrenia: an activation likelihood estimation meta-analysis of illness progression. Schizophr. Bull. 37, 177– 188 10.1093/schbul/sbp073 19633214 PMC3004195 · DOI
- Franklin B. J. Paxinos G. (2008). The Mouse Brain in Stereotaxic Coordinates. New York: Academic Press
- Authors
- Steullet, P., Cabungcal, J.-H., Cuénod, M., & Do, K. Q.
- Affiliations
- Centre Hospitalier Universitaire Vaudois (CH)
- Corresponding author
- Steullet, Pascal
- ORCID
- Steullet, Pascal
- Venue
- Frontiers in Cellular Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2014-08-20
- Volume
- 8
- Pages
- 244-244
- ISSN
- 1662-5102 (ISSN-L)
- PMC
- PMC4139002
- OpenAlex
- W2082769948
- Cited by
- 49
- References
- 78
- Citations by year
- 2025: 4 · 2024: 5 · 2023: 3 · 2022: 5 · 2021: 8 · 2020: 3 · 2019: 1 · 2018: 5 · 2017: 5 · 2016: 4 · 2015: 6
- FWCI
- 2.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Cellular Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- IRIS (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (310030_135736/1, 135736, 310030)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- anterior cingulate cortex, dopamine, beta oscillations, high-frequency oscillations, perineuronal nets, parvalbumin interneurons, dopamine D2 receptor, dopamine D1 receptor, dopamine D4 receptor, gap junctions, kainic acid, carbachol, schizophrenia, neuronal network activity
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