Neocortical Network Activity In Vivo Is Generated through a Dynamic Balance of Excitation and Inhibition
Open accessAbstract
The recurrent excitatory and inhibitory connections between and within layers of the cerebral cortex are fundamental to the operation of local cortical circuits. Models of cortical function often assume that recurrent excitation and inhibition are balanced, and we recently demonstrated that spontaneous network activity in vitro contains a precise balance of excitation and inhibition; however, the existence of a balance between excitation and inhibition in the intact and spontaneously active cerebral cortex has not been directly tested. We examined this hypothesis in the prefrontal cortex in vivo, during the slow (<1 Hz) oscillation in ketamine–xylazine-anesthetized ferrets. We measured persistent network activity (Up states) with extracellular multiple unit and local field potential recording, while simultaneously recording synaptic currents in nearby cells. We determined the reversal potential and conductance change over time during Up states and found that the body of Up state activity exhibited a steady reversal potential (−37 mV on average) for hundreds of milliseconds, even during substantial (21 nS on average) changes in membrane conductance. Furthermore, we found that both the initial and final segments of the Up state were characterized by significantly more depolarized reversal potentials and concomitant increases in excitatory conductance, compared with the stable middle portions of Up states. This ongoing temporal evolution between excitation and inhibition, which exhibits remarkable proportionality within and across neurons in active local networks, may allow for rapid transitions between relatively stable network states, permitting the modulation of neuronal responsiveness in a behaviorally relevant manner.
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The up-state reflects some balance between excitatory and inhibitory neuronal activity, whereas the hyperpolarizing down-state represents a period of disfacilitation that does not contain active inhibition.
“Whereas the up-state reflects some balance between excitatory and inhibitory neuronal activity (505, 1017, 1074), the hyperpolarizing down-state represents a period of disfacilitation that does not contain active inhibition (229,1146).”
From About Sleep's Role in Memory (2013) · cites this paper as [505]
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Neural Network Mechanisms Underlying Stimulus Driven Variability Reduction
Deco, G., & Hugues, E. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002395 · Cited by 132 · see citing works
The microcircuit concept applied to cortical evolution: from three-layer to six-layer cortex
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Activity regulates cell death within cortical interneurons through a Calcineurin-dependent mechanism
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Enhancement of visual responsiveness by spontaneous local network activity in vivo
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Self-citationNeocortical networks entrain neuronal circuits in cerebellar cortex
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Contrast gain control and horizontal interactions in V1: A DCM study
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Hyperexcitability and homeostasis in fragile X Syndrome.
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- Authors
- Haider, B., Duque, A., Hasenstaub, A. R., & McCormick, D. A.
- Affiliations
- Yale University (US)
- Corresponding author
- McCormick, David A.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-04-26
- Volume
- 26
- Issue
- 17
- Pages
- 4535-4545
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6674060
- OpenAlex
- W2100438317
- Cited by
- 962
- References
- 65
- Citations by year
- 2026: 24 · 2025: 34 · 2024: 34 · 2023: 36 · 2022: 48 · 2021: 46 · 2020: 87 · 2019: 54 · 2018: 35 · 2017: 60 · 2016: 50 · 2015: 54 · 2014: 68 · 2013: 54 · 2012: 45
- FWCI
- 21.50
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Kavli Foundation
- Pfizer
- National Institutes of Health
- 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 › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- excitation-inhibition balance, prefrontal cortex, slow oscillations, up states, reversal potential, synaptic conductance, spontaneous network activity, ferrets, local field potentials
- MeSH terms
- Action Potentials, Animals, Biological Clocks, Cells, Cultured, Computer Simulation, Ferrets, Male, Models, Neurological, Nerve Net, Neural Inhibition, Synaptic Transmission, Neurons, Neocortex, Excitatory Postsynaptic Potentials
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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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