Neocortical excitation/inhibition balance in information processing and social dysfunction
Open accessAbstract
Severe behavioural deficits in psychiatric diseases such as autism and schizophrenia have been hypothesized to arise from elevations in the cellular balance of excitation and inhibition (E/I balance) within neural microcircuitry. This hypothesis could unify diverse streams of pathophysiological and genetic evidence, but has not been susceptible to direct testing. Here we design and use several novel optogenetic tools to causally investigate the cellular E/I balance hypothesis in freely moving mammals, and explore the associated circuit physiology. Elevation, but not reduction, of cellular E/I balance within the mouse medial prefrontal cortex was found to elicit a profound impairment in cellular information processing, associated with specific behavioural impairments and increased high-frequency power in the 30-80 Hz range, which have both been observed in clinical conditions in humans. Consistent with the E/I balance hypothesis, compensatory elevation of inhibitory cell excitability partially rescued social deficits caused by E/I balance elevation. These results provide support for the elevated cellular E/I balance hypothesis of severe neuropsychiatric disease-related symptoms.
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Conventionally used AAV backbones with a 1.3 kb CaMKIIα promoter, WPRE, and human growth hormone polyadenylation signal have a capacity of 2.4 kb.
“Conventionally used AAV backbones which include a commonly used neuronal expression cassette composed of 1.3 kb CaMKIIα promoter (which shows comparable expression efficiency with 0.4 kb CaMKIIα promoter [10] used in CWB), WPRE, and human growth hormone polyadenylation signal [23-25] has a capacity of 2.4 kb.”
From Optimization of AAV expression cassettes to improve packaging capacity and transgene expression in neurons (2014) · cites this paper as [24]
The Consequences of altered E/I balance section describes an AAV expressing SSFO–EYFP under a CaMKIIα promoter, supporting the use of that promoter in an AAV construct. The passages do not specify a 1.3 kb promoter, WPRE, a human growth hormone polyadenylation signal, or a 2.4 kb capacity; searches for those terms found no supporting passage. Page numbers were unavailable in our copy. (LLM, conf=0.83)
Experimental — accuracy not yet measuredAlterations in the balance between excitatory and inhibitory signalling in neural micro-circuitry have been implicated in social deficits as seen in ASD and SCZ.
“Importantly, alterations in the balance between excitatory and inhibitory signalling in neural micro-circuitry have been implicated in social deficits as seen in ASD and SCZ (Yizhar et al. 2011).”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Yizhar et al. 2011
Changes in PFC network activity directly affect cognitive and social skills.
“Changes in PFC network activity directly affect cognitive and social skills”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Yizhar et al., 2011
Elevated levels of the repressive H3K27me3 mark, catalyzed by EZH2, have been observed in chronic stress models.
“Elevated levels of the repressive H3K27me3 mark, catalyzed by the histone methyltransferase EZH2, have also been observed in chronic stress models.”
From Histone modifications and depression: epigenetic mechanisms, therapeutic targets, and translational outlook (2026) · cites this paper as Yizhar et al., 2011
The Consequences of altered E/I balance and Discussion passages concern optogenetic changes in cortical excitation and inhibition, not histone marks or chronic stress models. Searches for H3K27me3, EZH2, and stress-related epigenetic modification found no passage addressing the claim. Page numbers were not available in our copy. (LLM, conf=0.78)
Experimental — accuracy not yet measuredThese increases are associated with reduced expression of neuroplasticity-related genes, including CREB and enzymes involved in GABA synthesis.
“These increases are associated with reduced expression of neuroplasticity-related genes, including CREB and enzymes involved in GABA synthesis (Yizhar et al., 2011).”
From Histone modifications and depression: epigenetic mechanisms, therapeutic targets, and translational outlook (2026) · cites this paper as Yizhar et al., 2011
The Discussion describes elevated excitation/inhibition balance and increased gamma power, but does not link either increase to reduced gene expression. Searches for CREB, neuroplasticity-related genes, and GABA-synthesis enzymes found no passage reporting the claimed association; the References list GABA-related gene-expression studies but do not establish it here. (LLM, conf=0.74)
Experimental — accuracy not yet measured
Psychotic symptoms may be seen as attempts to garner some advantage, perhaps by convincing others of their veracity.
“Psychotic symptoms may be seen as attempts to garner some advantage, perhaps by convincing others of their veracity (113).”
From The Predictive Coding Account of Psychosis (2018) · cites this paper as [113]
The Abstract and Discussion describe neural excitation/inhibition balance, information processing, and social dysfunction in mice. Searches for psychotic symptoms as attempts to gain an advantage or convince others found no passage addressing that interpretation. (LLM, conf=0.76)
Experimental — accuracy not yet measuredDefective synaptic function leading to an excitation-inhibition imbalance is commonly invoked as one possible explanation for ASD and is supported by evidence in humans and rodents.
“Defective synaptic function leading to an excitation–inhibition (E/I) imbalance is commonly invoked as one possible explanation for ASD (Rubenstein and Merzenich 2003), and is supported by evidence in humans and rodents (Yizhar et al. 2011; Hashemi et al. 2017; Selimbeyoglu et al. 2017).”
From Dysfunctional Autism Risk Genes Cause Circuit-Specific Connectivity Deficits With Distinct Developmental Trajectories (2018) · cites this paper as Yizhar et al. 2011
Increased neural excitability can lead to impairments in social interaction and cognitive functions in a mouse model of autism.
“Yizhar et al. (2011) have shown that increased neural excitability can lead to impairments in social interaction and cognitive functions in a mouse model of autism.”
From From early markers to neuro-developmental mechanisms of autism (2014) · cites this paper as Yizhar et al., 2011
Changes in mTOR-autophagy signaling and spine pruning defects may represent a secondary mechanism in response to an imbalance between excitatory and inhibitory neurotransmission.
“changes in mTOR-autophagy signaling and spine pruning defects may represent a secondary mechanism in response to an imbalance between excitatory and inhibitory neurotransmission”
From Loss of mTOR-Dependent Macroautophagy Causes Autistic-like Synaptic Pruning Deficits (2014) · cites this paper as Yizhar et al., 2011
Increasing neural excitation is sufficient to disrupt cognition and sociability.
“Recently, it was demonstrated that increasing neural excitation is sufficient to disrupt cognition and sociability”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Yizhar et al., 2011
Elevated excitation is sufficient to disrupt cognition and sociability.
“E/I imbalance is a defining neurophysiological feature of neurodevelopmental disorders (Rubenstein and Merzenich, 2003) and elevated excitation is sufficient to disrupt cognition and sociability (Yizhar et al., 2011).”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Yizhar et al., 2011
Laser stimulation of PV cINs expressing C1V1 resulted in firing time-locked to the stimulus.
“both constant and high frequency laser stimulation of PV cINs expressing the red-shifted opsin C1V1 in brain slices40 resulted in firing time-locked to the stimulus.”
From Viral manipulation of functionally distinct interneurons in mice, non-human primates and humans (2020) · cites this paper as [40]
In mice, both congenital knockout and haploinsufficiency of Shank3 lead to diminished social interest in others and are associated with disruption of cortical and subcortical circuits thought to be involved in ASD and its ontogenesis.
“In mice, both congenital knockout and haploinsufficiency of Shank3 leads to diminished social interest in others and is associated with the disruption of cortical and subcortical circuits thought to be involved in ASD 22–26 and its ontogenesis 22,25,27,28.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [26]
The mPFC is an area suggested to be involved in social behavior and disorders such as ASD.
“Here, we used microelectrode arrays that were implanted in the animal’s mPFC (Extended Data Fig. 1b), an area suggested to be involved in social behavior 1,7,12,26,34 and disorders such as ASD 14,21,35,36.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [26]
SSFO upon activation by a single light pulse leads to prolonged (approximately 30 min) sub-threshold depolarization, sensitizing the cell to afferent inputs rather than inducing firing directly.
“we chose to use the Stabilized Step Function Opsin (SSFO), which upon activation by a single light pulse leads to prolonged (approximately 30 min) sub-threshold depolarization (Yizhar et al., 2011), sensitizing the cell to afferent inputs rather than inducing firing directly.”
From Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors (2020) · cites this paper as Yizhar et al., 2011
The device produces sufficient light intensity for effective activation of considerable target volumes using SSFO, with an estimated 1.75 mm3 of brain tissue illuminated above 8 microwatt×mm-2, the lowest reported functional light intensity for SSFO.
“This provided an estimated 1.75 mm3 of brain tissue being illuminated with light intensity above 8 microwatt×mm–2, the lowest reported functional light intensity for SSFO”
From Wireless Optogenetic Stimulation of Oxytocin Neurons in a Semi-natural Setup Dynamically Elevates Both Pro-social and Agonistic Behaviors (2020) · cites this paper as Yizhar et al., 2011
Elevated mPFC activity results in ASD-related phenotypes, and decreasing mPFC activity is sufficient to rescue abnormal behaviors in ASD models.
“Neural circuit manipulation in combination with neural recordings provide direct evidence that elevated mPFC activity results in ASD-related phenotypes, whereas decreasing mPFC activity is sufficient to rescue abnormal behaviors in ASD models22,23,24.”
From Regulation of autism-relevant behaviors by cerebellar-prefrontal cortical circuits (2020) · cites this paper as [23]
Our integrative analyses have allowed us to identify disease-relevant cell types for a disorder, identify unique dysfunctions in individual cohorts, and deduce a potential functional basis of a disorder based on the cells affected.
“Our integrative analyses have allowed us to: (a) identify disease-relevant cell types for a disorder; (b) identify unique dysfunctions in individual cohorts (due to impact on very specific subtypes); (c) deduce a potential functional basis of a disorder (such as excitatory/inhibitory balance48,49, lack of myelination50 etc.) based on the cells affected.”
From Cell type-specific transcriptional programs in mouse prefrontal cortex during adolescence and addiction (2019) · cites this paper as [49]
Disruption of E/I balance can give rise to profound behavioral deficits and may play a key role in schizophrenia.
“Disruption of the ratio of excitation and inhibition (E/I balance) can give rise to profound behavioral deficits and may play a key role in serious mental illnesses such as schizophrenia (Yizhar et al. 2011).”
From Linking microcircuit dysfunction to cognitive impairment: Effects of disinhibition associated with schizophrenia in a cortical working memory model (2014) · cites this paper as Yizhar et al. 2011
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“For example, optogenetic manipulation of E/I balance (113) could be used to explore the computations underlying predictive coding.”
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- Authors
- Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O’Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., Stehfest, K., Fudim, R., Ramakrishnan, C., Huguenard, J. R., Hegemann, P., & Deisseroth, K.
- Affiliations
- Stanford University (US)
- Humboldt-Universität zu Berlin (DE)
- University of California, San Francisco (US)
- Stanford Medicine (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Yizhar, Ofer
- Hegemann, Peter
- Deisseroth, Karl
- ORCID
- Venue
- Nature
- Published
- 2011-07-27
- Volume
- 477
- Issue
- 7363
- Pages
- 171-178
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4155501
- OpenAlex
- W2072652550
- Cited by
- 2,454
- References
- 51
- Citations by year
- 2026: 138 · 2025: 154 · 2024: 154 · 2023: 193 · 2022: 179 · 2021: 202 · 2020: 183 · 2019: 172 · 2018: 186 · 2017: 165 · 2016: 152 · 2015: 173 · 2014: 143 · 2013: 129 · 2012: 107
- FWCI
- 52.83
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (DP1OD000616)
- National Institute of Mental Health (R01MH075957, R01MH086373)
- National Institute of Neurological Disorders and Stroke (R01NS034774, R01NS006477)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- excitation-inhibition balance, medial prefrontal cortex, social dysfunction, autism spectrum disorder, schizophrenia, neuropsychiatric disorders, optogenetics, inhibitory interneurons, neuronal excitability, high-frequency oscillations, social behavior, learning behavior
- MeSH terms
- Animals, Autistic Disorder, Mental Disorders, Disease Models, Animal, Hippocampus, Humans, Learning, Models, Neurological, Motor Activity, Neural Inhibition, Neurons, Schizophrenia, Social Behavior, Prefrontal Cortex, Mice, Opsins, HEK293 Cells
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.
What counts as a claim ›How we measure confidence ›How we check this ›
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