Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia

Lisman, John E.; Coyle, Joseph T.; Green, Robert W.; Javitt, Daniel C.; Benes, Francine M.; Heckers, Stephan; Grace, Anthony A.

doi:10.1016/j.tins.2008.02.005

Cited by 1,010Schizophrenia research and treatmentNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia

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Lisman, John E., Coyle, Joseph T., Green, Robert W., Javitt, Daniel C., Benes, Francine M., Heckers, Stephan, Grace, Anthony A.·2008·Trends in Neurosciences

DOI 10.1016/j.tins.2008.02.005PMC PMC2680493

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Abstract

Many risk genes interact synergistically to produce schizophrenia and many neurotransmitter interactions have been implicated. We have developed a circuit-based framework for understanding gene and neurotransmitter interactions. NMDAR hypofunction has been implicated in schizophrenia because NMDAR antagonists reproduce symptoms of the disease. One action of antagonists is to reduce the excitation of fast-spiking interneurons, resulting in disinhibition of pyramidal cells. Overactive pyramidal cells, notably those in the hippocampus, can drive a hyperdopaminergic state that produces psychosis. Additional aspects of interneuron function can be understood in this framework, as follows. (i) In animal models, NMDAR antagonists reduce parvalbumin and GAD67, as found in schizophrenia. These changes produce further disinhibition and can be viewed as the aberrant response of a homeostatic system having a faulty activity sensor (the NMDAR). (ii) Disinhibition decreases the power of gamma oscillation and might thereby produce negative and cognitive symptoms. (iii) Nicotine enhances the output of interneurons, and might thereby contribute to its therapeutic effect in schizophrenia.

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Compelling evidence suggests an imbalance between glutamatergic excitation and GABAergic inhibition in schizophrenia.
“Compelling evidence suggests an imbalance between glutamatergic excitation and GABAergic inhibition in schizophrenia (Lisman et al., 2008; O’Donnell, 2011).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Lisman et al., 2008
In schizophrenia, NMDA receptors are believed to be hypo-functioning, and NMDA receptor inhibition reproduces many schizophrenia symptoms.
“In schizophrenia, NMDA receptors are believed to be hypo-functioning, and the inhibition of NMDA receptors recapitulates many of the symptoms of schizophrenia [104, 122, 123].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [123]
NMDA receptor antagonists such as ketamine and phencyclidine can transiently reproduce key clinical features of schizophrenia and are believed to reduce PV-IN excitation.
“NMDA receptor antagonists, such as ketamine and phencyclidine, can transiently reproduce key clinical features of schizophrenia, and are believed to reduce PV-IN excitation [123].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [123]
This mechanism may be linked to pathophysiology of schizophrenia and possibly accounts for some key effects of NMDAR antagonists such as ketamine.
“This mechanism may be linked to the pathophysiology of schizophrenia (Lisman et al. 2008;Nakazawa et al. 2012) and possibly accounts for some of the key effects of NMDAR antagonists, such as ketamine, which are a leading pharmacological model of schizophrenia (Krystal et al. 1994).”
From Linking microcircuit dysfunction to cognitive impairment: Effects of disinhibition associated with schizophrenia in a cortical working memory model (2014) · cites this paper as Lisman et al. 2008
Elevated prefrontal E/I ratio may result from alterations in multiple pathways implicated in schizophrenia, including GABAergic deficits, increased background input from other areas, or abnormal levels of neuromodulators.
“Elevated prefrontal E/I ratio may result from alterations in multiple pathways that are implicated in schizophrenia.These include GABAergic deficits, such as reduced GAD67 production (Lewis et al. 2005); increased background input from other areas such as the thalamus or hippocampus (Lisman et al. 2008); or abnormal levels of neuromodulators (Laruelle et al. 2003).”
From Linking microcircuit dysfunction to cognitive impairment: Effects of disinhibition associated with schizophrenia in a cortical working memory model (2014) · cites this paper as Lisman et al. 2008

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“Of note, as far as we are aware, this is the first experimental demonstration that “neonatal” interaction of major genetic and environmental susceptibility factors for schizophrenia results in the dramatic change in the parvalbumin-positive interneurons in the medial prefrontal cortex (mPFC), one of the best hallmarks…”
Background
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Lower gene expression for KCNS3 potassium channel subunit in parvalbumin-containing neurons in the prefrontal cortex in schizophrenia
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On the Myelination of GABAergic Interneurons
Stedehouder, J. (2019) · RePub (Erasmus University Rotterdam)

Authors: Lisman, J. E., Coyle, J. T., Green, R. W., Javitt, D. C., Benes, F. M., Heckers, S., & Grace, A. A.
Affiliations: Brandeis University (US)
Harvard University (US)
The University of Texas Southwestern Medical Center (US)
Nathan Kline Institute for Psychiatric Research (US)
McLean Hospital (US)
Vanderbilt University (US)
University of Pittsburgh (US)
ORCID: Lisman, John E.
Coyle, Joseph T.
Javitt, Daniel C.
Benes, Francine M.
Heckers, Stephan
Grace, Anthony A.
Venue: Trends in Neurosciences
Publisher: Elsevier BV
Published: 2008-05
Volume: 31
Issue: 5
Pages: 234-242
ISSN: 0166-2236 (ISSN-L)
DOI: 10.1016/j.tins.2008.02.005
PMC: PMC2680493
OpenAlex: W2022809683
Cited by: 1,010
References: 161
Citations by year: 2026: 23 · 2025: 35 · 2024: 36 · 2023: 31 · 2022: 27 · 2021: 44 · 2020: 51 · 2019: 48 · 2018: 43 · 2017: 48 · 2016: 67 · 2015: 71 · 2014: 83 · 2013: 76 · 2012: 76
FWCI: 10.77
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Neurosciences (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: U.S. Department of Veterans Affairs
National Institutes of Health (5r01mh031862-24, MH070560, MH60450, MH42261, 5r01mh070560-16)
National Institute of Mental Health (R01MH042261, P50MH060450, R01MH051290, MH067999, MH31862, R01MH067999, R01-MH070560, MH-60450, MH-42261, R37MH042261, MH070560)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: schizophrenia, gene-gene interaction, neurotransmitter interactions, NMDA receptor hypofunction, NMDA receptor antagonists, fast-spiking interneurons, disinhibition, pyramidal neurons, hippocampus, hyperdopaminergic state, psychosis, parvalbumin, GAD67, gamma oscillations, negative symptoms, cognitive symptoms, nicotine, homeostatic regulation
MeSH terms: Animals, Cognition, Dopamine, gamma-Aminobutyric Acid, Hippocampus, Homeostasis, Humans, Nerve Net, Risk, Schizophrenia, Gene Expression, Receptors, N-Methyl-D-Aspartate, N-Methylaspartate, Neurotransmitter Agents

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