Functional maturation of GABA synapses during postnatal development of the monkey dorsolateral prefrontal cortex
Open accessAbstract
Development of inhibition onto pyramidal cells may be crucial for the emergence of cortical network activity, including gamma oscillations. In primate dorsolateral prefrontal cortex (DLPFC), inhibitory synaptogenesis starts in utero and inhibitory synapse density reaches adult levels before birth. However, in DLPFC, the expression levels of γ-aminobutyric acid (GABA) synapse-related gene products changes markedly during development until young adult age, suggesting a highly protracted maturation of GABA synapse function. Therefore, we examined the development of GABA synapses by recording GABAAR-mediated inhibitory postsynaptic currents (GABAAR-IPSCs) from pyramidal cells in the DLPFC of neonatal, prepubertal, peripubertal, and adult macaque monkeys. We found that the decay of GABAAR-IPSCs, possibly including those from parvalbumin-positive GABA neurons, shortened by prepubertal age, while their amplitude increased until the peripubertal period. Interestingly, both GABAAR-mediated quantal response size, estimated by miniature GABAAR-IPSCs, and the density of GABAAR synaptic appositions, measured with immunofluorescence microscopy, were stable with age. Simulations in a computational model network with constant GABA synapse density showed that the developmental changes in GABAAR-IPSC properties had a significant impact on oscillatory activity and predicted that, whereas DLPFC circuits can generate gamma frequency oscillations by prepubertal age, mature levels of gamma band power are attained at late stages of development.
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Inhibition onto pyramidal cells increases between juvenile and adolescent/adult groups in both mice and macaques.
“In contrast, inhibition onto pyramidal cells increases between juvenile and adolescent/adult groups in both mice and macaques (Delevich, 2014; Gonzalez-Burgos et al., 2015; Vandenberg et al., 2015).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Gonzalez-Burgos et al., 2015
Inhibitory current amplitudes increase around puberty in rhesus macaque dlPFC.
“and inhibitory current amplitudes increase around puberty in rhesus macaque dlPFC (Gonzalez-Burgos et al., 2015).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Gonzalez-Burgos et al., 2015
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Synaptic Variability and Cortical Gamma Oscillation Power in Schizophrenia
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Dysregulated Prefrontal Cortex Inhibition in Prepubescent and Adolescent Fragile X Mouse Model
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Kalemaki, K., Velli, A., Christodoulou, O., Denaxa, M., Karagogeos, D., & Sidiropoulou, K. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab438 · Cited by 24 · see citing works
Working Memory: From Neural Activity to the Sentient Mind
Jaffe, R. J., & Constantinidis, C. (2021) · Comprehensive physiology · doi:10.1002/cphy.c210005 · Cited by 32 · see citing works
Hankosky, E. R., Westbrook, S. R., Haake, R. M., Willing, J., Raetzman, L. T., Juraska, J. M., & Gulley, J. M. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.04.047 · Cited by 23 · see citing works
Axonal CB1 Receptors Mediate Inhibitory Bouton Formation via cAMP Increase and PKA
Liang, J., Kruijssen, D. L. H., Verschuuren, A. C. J., Voesenek, B. J. B., Benavides, F. F. W., González, M. S., Ruiter, M., & Wierenga, C. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0851-21.2021 · Cited by 20 · see citing works
Plasticity of Persistent Activity and Its Constraints
Li, S., Zhou, X., Constantinidis, C., & Qi, X.-L. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.00015 · Cited by 22 · see citing works
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Functional properties of GABA synaptic inputs onto GABA neurons in monkey prefrontal cortex
Rotaru, D. C., Olezene, C. S., Miyamae, T., Povysheva, N. V., Zaitsev, A. V., Lewis, D. A., & González‐Burgos, G. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00799.2014 · Cited by 15 · see citing works
Strong Gamma Frequency Oscillations in the Adolescent Prefrontal Cortex
Wang, Z., Singh, B., Zhou, X., & Constantinidis, C. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1604-21.2022 · Cited by 11 · see citing works
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Working Memory: From Neural Activity to the Sentient Mind
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González‐Burgos, G., Miyamae, T., Nishihata, Y., Krimer, O. L., & Lewis, D. A. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.01.019 · Cited by 6 · see citing works
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- Authors
- Gonzalez-Burgos, G., Miyamae, T., Pafundo, D. E., Yoshino, H., Rotaru, D. C., Hoftman, G., Datta, D., Zhang, Y., Hammond, M., Sampson, A. R., Fish, K. N., Bard Ermentrout, G., & Lewis, D. A.
- Affiliations
- University of Pittsburgh (US)
- ORCID
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-06-05
- Volume
- 25
- Issue
- 11
- Pages
- 4076-4093
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC4626828
- OpenAlex
- W2108130753
- Cited by
- 64
- References
- 110
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 5 · 2023: 7 · 2022: 8 · 2021: 7 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 3 · 2016: 6 · 2015: 3 · 2014: 1
- FWCI
- 1.98
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cerebral Cortex (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (P50MH084053, MH084053, R01MH096985, MH051234, MH096985, R01MH051234)
- National Institute on Drug Abuse (DA-023109, R01DA023109)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- dorsolateral prefrontal cortex, postnatal development, GABAA receptor, inhibitory postsynaptic currents, pyramidal neurons, parvalbumin interneurons, gamma oscillations, miniature IPSCs, macaque, prepubertal development
- MeSH terms
- Age Factors, Animals, Animals, Newborn, Calcium Channel Blockers, Female, gamma-Aminobutyric Acid, Lysine, Macaca mulatta, Models, Neurological, Neurons, Pyridazines, Synapses, Prefrontal Cortex, alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid, Excitatory Amino Acid Agonists, Excitatory Amino Acid Antagonists, 6-Cyano-7-nitroquinoxaline-2,3-dione, GABA Antagonists, omega-Agatoxin IVA, 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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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