GABAergic interneurons in epilepsy: More than a simple change in inhibition
Jasper’s basic mechanisms of the epilepsies.
4th ed. 2012
Excitation and inhibition in epilepsy.
Can J Neurol Sci. 1996; 23: 167-174
Cellular mechanisms of epilepsy: a status report.
Science. 1987; 237: 157-164
Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex.
Nat Neurosci. 1998; 1: 587-594
Synaptic depression: a key player in the cortical balancing act.
Nat Neurosci. 1998; 1: 539-541
Electrophysiology of GABA-mediated synaptic transmission and possible roles in epilepsy.
Neurochem Res. 1991; 16: 251-262
Contribution of intrinsic neuronal factors in the generation of cortically driven electrographic seizures.
J Neurophysiol. 2004; 92: 1133-1143
Pediatric epilepsy mechanisms: expanding the paradigm of excitation/inhibition imbalance.
Children (Basel). 2019; 6
Dentate gyrus mossy cells control spontaneous convulsive seizures and spatial memory.
Science. 2018; 359: 787-790
GABA and epileptogenesis.
Epilepsia. 1997; 38: 399-407
GABAergic mechanisms in epilepsy.
Epilepsia. 2001; 42: 8-12
Hippocampal GABAergic inhibitory interneurons.
Physiol Rev. 2017; 97: 1619-1747
Inhibitory or excitatory? Optogenetic interrogation of the functional roles of GABAergic interneurons in epileptogenesis.
J Biomed Sci. 2017; 24: 93
Development and specification of GABAergic cortical interneurons.
Cell Biosci. 2013; 3: 19
Dysfunction of hippocampal interneurons in epilepsy.
Neurosci Bull. 2014; 30: 985-998
Laminar distribution of neurochemically-identified interneurons and cellular co-expression of molecular markers in epileptic human cortex.
Neurosci Bull. 2018; 34: 992-1006
The temporal and spatial origins of cortical interneurons predict their physiological subtype.
Neuron. 2005; 48: 591-604
Cortical interneurons and their origins.
Neuroscientist. 2005; 11: 199-205
Generation of interneuron diversity in the mouse cerebral cortex.
Eur J Neurosci. 2010; 31: 2136-2141
A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity.
J Neurosci. 2011; 31: 10948-10970
Origin of GABAergic neurons in the human neocortex.
Nature. 2002; 417: 645-649
Extended production of cortical interneurons into the third trimester of human gestation.
Cereb Cortex. 2016; 26: 2242-2256
Role of GABAergic inhibition in hippocampal network oscillations.
Trends Neurosci. 2007; 30: 343-349
Interneurons of the hippocampus.
Hippocampus. 1996; 6: 347-470
Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations.
Science. 2008; 321: 53-57
Differences between somatic and dendritic inhibition in the hippocampus.
Neuron. 1996; 16: 815-823
Highly specific structural plasticity of inhibitory circuits in the adult neocortex.
Neuroscientist. 2013; 19: 384-393
Global optogenetic activation of inhibitory interneurons during epileptiform activity.
J Neurosci. 2014; 34: 3364-3377
Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons.
Nature. 1995; 378: 75-78
Paired recordings from neurones.
Curr Opin Neurobiol. 1996; 6: 387-394
Quantitative dynamics and spatial profile of perisomatic GABAergic input during epileptiform synchronization in the CA1 hippocampus.
J Physiol. 2009; 587: 5691-5708
Lighting the chandelier: new vistas for axo-axonic cells.
Trends Neurosci. 2005; 28: 310-316
Molecular specialization of GABAergic synapses on the soma and axon in cortical and hippocampal circuit function and dysfunction.
Front Mol Neurosci. 2019; 12: 154
Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms.
J Neurosci. 1995; 15: 30-46
Diversity of inhibitory neurotransmission through GABA(A) receptors.
Trends Neurosci. 2004; 27: 569-575
Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro.
Neuron. 2005; 45: 105-117
Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo.
J Neurosci. 2007; 27: 8184-8189
GABAergic cell subtypes and their synaptic connections in rat frontal cortex.
Cereb Cortex. 1997; 7: 476-486
GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus.
Eur J Neurosci. 2009; 30: 947-957
OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons.
Nat Neurosci. 2012; 15: 1524-1530
Dendritic inhibition mediated by O-LM and bistratified interneurons in the hippocampus.
Front Synaptic Neurosci. 2014; 6: 23
The interneuron energy hypothesis: implications for brain disease.
Neurobiol Dis. 2016; 90: 75-85
Generating neuronal diversity in the mammalian cerebral cortex.
Annu Rev Cell Dev Biol. 2015; 31: 699-720
On the origin of interictal activity in human temporal lobe epilepsy in vitro.
Science. 2002; 298: 1418-1421
Epileptogenic actions of GABA and fast oscillations in the developing hippocampus.
Neuron. 2005; 48: 787-796
Regional specificity of chandelier neuron axon terminal alterations in schizophrenia.
Neuroscience. 2006; 138: 189-196
Transient depression of excitatory synapses on interneurons contributes to epileptiform bursts during gamma oscillations in the mouse hippocampal slice.
J Neurophysiol. 2005; 94: 1225-1235
Inhibition and oscillations in the human brain tissue in vitro.
Neurobiol Dis. 2019; 125: 198-210
Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia.
J Neurosci. 2005; 25: 9649-9657
Interneuron dysfunction in psychiatric disorders.
Nat Rev Neurosci. 2012; 13: 107-120
GABAergic interneuron origin of schizophrenia pathophysiology.
Neuropharmacology. 2012; 62: 1574-1583
Alteration of GABAergic signaling is associated with anxiety-like behavior in temporal lobe epilepsy mice.
Prog Neuropsychopharmacol Biol Psychiatry. 2019; 93: 141-148
Developmental abnormalities of cortical interneurons precede symptoms onset in a mouse model of Rett syndrome.
J Neurochem. 2014; 131: 115-127
X-linked lissencephaly with abnormal genitalia as a tangential migration disorder causing intractable epilepsy: proposal for a new term, “interneuronopathy”.
J Child Neurol. 2005; 20: 392-397
The promise of an interneuron-based cell therapy for epilepsy.
Dev Neurobiol. 2011; 71: 107-117
Interneuron deficits in neurodevelopmental disorders: implications for disease pathology and interneuron-based therapies.
Eur J Paediatr Neurol. 2019; ([In Press])https://doi.org/10.1016/j.ejpn.2019.12.015
Interneuronophaties and their role in the early life epilepsies and neurodevelopmental disorders.
Epilepsia Open. 2017; 2: 284-306
Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study.
Arch Gen Psychiatry. 2000; 57: 1061-1069
Cell-type specific alterations of cortical interneurons in schizophrenic patients.
Neuroreport. 2002; 13: 713-717
Epilepsy following cortical injury: cellular and molecular mechanisms as targets for potential prophylaxis.
Epilepsia. 2009; 50: 30-40
Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation.
Arch Gen Psychiatry. 2002; 59: 347-354
Neural synchrony indexes disordered perception and cognition in schizophrenia.
Proc Natl Acad Sci U S A. 2004; 101: 17288-17293
The role of GABA in the pathophysiology and treatment of anxiety disorders.
Psychopharmacol Bull. 2003; 37: 133-146
Long-lasting anxiolytic effect of neural precursor cells freshly prepared but not neurosphere-derived cell transplantation in newborn rats.
BMC Neurosci. 2014; 15: 94
Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study.
J Autism Dev Disord. 2001; 31: 537-543
Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices.
Biol Psychiatry. 2002; 52: 805-810
Neurobiological bases of autism-epilepsy comorbidity: a focus on excitation/inhibition imbalance.
Eur J Neurosci. 2018; 47: 534-548
Common circuit defect of excitatory-inhibitory balance in mouse models of autism.
J Neurodev Disord. 2009; 1: 172-181
Model of autism: increased ratio of excitation/inhibition in key neural systems.
Genes Brain Behav. 2003; 2: 255-267
Dissecting the phenotypes of Dravet syndrome by gene deletion.
Brain. 2015; 138: 2219-2233
Loss of GABAergic neurons in the hippocampus and cerebral cortex of engrailed-2 null mutant mice: implications for autism spectrum disorders.
Exp Neurol. 2013; 247: 496-505
Resveratrol prevents cellular and behavioral sensory alterations in the animal model of autism induced by valproic acid.
Front Synaptic Neurosci. 2018; 10: 9
Epilepsy in autism spectrum disorders.
Eur Child Adolesc Psychiatry. 2007; 16: 61-66
Autistic spectrum disorder: evaluating a possible contributing or causal role of epilepsy.
Epilepsia. 2006; 47: 79-82
Epilepsy and EEG paroxysmal abnormalities in autism spectrum disorders.
Brain Dev. 2010; 32: 783-789
Epilepsy as a spectrum disorder: implications from novel clinical and basic neuroscience.
Epilepsia. 2011; 52: 1-6
Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology.
Neuron. 2006; 52: 155-168
High frequency oscillations in the intact brain.
Prog Neurobiol. 2012; 98: 241-249
Driving fast-spiking cells induces gamma rhythm and controls sensory responses.
Nature. 2009; 459: 663-667
NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex.
Proc Natl Acad Sci U S A. 2008; 105: 18572-18577
Interneuron diversity series: inhibitory interneurons and network oscillations in vitro.
Trends Neurosci. 2003; 26: 676-682
Cortical gamma band synchronization through somatostatin interneurons.
Nat Neurosci. 2017; 20: 951-959
Basal forebrain somatostatin cells differentially regulate local gamma oscillations and functionally segregate motor and cognitive circuits.
Sci Rep. 2019; 9: 2570
Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations.
Neuron. 2014; 83: 467-480
Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks.
Proc Natl Acad Sci U S A. 2002; 99: 13222-13227
Reorganization of barrel circuits leads to thalamically-evoked cortical epileptiform activity.
Thalamus Relat Syst. 2005; 3: 261-273
A new mode of corticothalamic transmission revealed in the gria4(−/−) model of absence epilepsy.
Nat Neurosci. 2011; 14: 1167-1173
Microcircuits and their interactions in epilepsy: is the focus out of focus?.
Nat Neurosci. 2015; 18: 351-359
Parvalbumin-positive inhibitory interneurons oppose propagation but favor generation of focal epileptiform activity.
J Neurosci. 2015; 35: 9544-9557
Selective silencing of hippocampal parvalbumin interneurons induces development of recurrent spontaneous limbic seizures in mice.
J Neurosci. 2017; 37: 8166-8179
Rapid rebalancing of excitation and inhibition by cortical circuitry.
Neuron. 2018; 97: 1341-1355.e6
Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy.
Nat Neurosci. 2005; 8: 1059-1068
Calretinin immunoreactivity in focal cortical dysplasias and in non-malformed epileptic cortex.
Epilepsy Res. 2010; 88: 76-86
Surviving CA1 pyramidal cells receive intact perisomatic inhibitory input in the human epileptic hippocampus.
Brain. 2005; 128: 138-152
Loss and reorganization of calretinin-containing interneurons in the epileptic human hippocampus.
Brain. 2010; 133: 2763-2777
Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures.
J Comp Neurol. 2003; 459: 407-425
Alterations in hippocampal and cortical densities of functionally different interneurons in rat models of absence epilepsy.
Epilepsy Res. 2018; 145: 40-50
Loss of hippocampal interneurons and epileptogenesis: a comparison of two animal models of acquired epilepsy.
Brain Struct Funct. 2015; 220: 153-191
Selective loss of dentate hilar interneurons contributes to reduced synaptic inhibition of granule cells in an electrical stimulation-based animal model of temporal lobe epilepsy.
J Comp Neurol. 2007; 500: 876-893
Impaired and repaired inhibitory circuits in the epileptic human hippocampus.
Trends Neurosci. 2005; 28: 334-340
A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy.
Ann Neurol. 1991; 29: 325-332
Somatostatin- and neuropeptide Y-synthesizing neurones in the fascia dentata of humans with temporal lobe epilepsy.
Brain. 2001; 124: 688-697
Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy.
J Neurosci. 2003; 23: 2440-2452
Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy.
Nat Neurosci. 2001; 4: 52-62
Synaptic reorganization of the perisomatic inhibitory network in hippocampi of temporal lobe epileptic patients.
Biomed Res Int. 2017; 20177154295
Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus.
Neuroscience. 2001; 108: 587-600
A reorganized GABAergic circuit in a model of epilepsy: evidence from optogenetic labeling and stimulation of somatostatin interneurons.
J Neurosci. 2013; 33: 14392-14405
Surviving hilar somatostatin interneurons enlarge, sprout axons, and form new synapses with granule cells in a mouse model of temporal lobe epilepsy.
J Neurosci. 2009; 29: 14247-14256
Axonal sprouting in commissurally projecting parvalbumin-expressing interneurons.
J Neurosci Res. 2017; 95: 2336-2344
Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy.
Brain Res. 1989; 495: 387-395
Synaptic interactions between pyramidal cells and interneurone subtypes during seizure-like activity in the rat hippocampus.
J Physiol. 2004; 557: 961-979
Natural waking and sleep states: a view from inside neocortical neurons.
J Neurophysiol. 2001; 85: 1969-1985
Impact of intrinsic properties and synaptic factors on the activity of neocortical networks in vivo.
J Physiol Paris. 2000; 94: 343-355
Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study.
Proc Natl Acad Sci U S A. 2001; 98: 1924-1929
Inhibition dominates sensory responses in the awake cortex.
Nature. 2013; 493: 97-100
Impact of network activities on neuronal properties in corticothalamic systems.
J Neurophysiol. 2001; 86: 1-39
Contribution of parvalbumin and somatostatin-expressing GABAergic neurons to slow oscillations and the balance in beta-gamma oscillations across cortical layers.
Front Neural Circuits. 2015; 9: 6
Selective activation of parvalbumin- or somatostatin-expressing interneurons triggers epileptic seizurelike activity in mouse medial entorhinal cortex.
J Neurophysiol. 2015; 113: 1616-1630
Early GABAergic circuitry in the cerebral cortex.
Curr Opin Neurobiol. 2014; 26: 72-78
Giant synaptic potentials in immature rat CA3 hippocampal neurones.
J Physiol. 1989; 416: 303-325
GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations.
Physiol Rev. 2007; 87: 1215-1284
Excitatory actions of gaba during development: the nature of the nurture.
Nat Rev Neurosci. 2002; 3: 728-739
Sequential generation of two distinct synapse-driven network patterns in developing neocortex.
J Neurosci. 2008; 28: 12851-12863
Mechanisms and effects of seizures in the immature brain.
Semin Fetal Neonatal Med. 2013; 18: 175-184
Unit activity of hippocampal interneurons before spontaneous seizures in an animal model of temporal lobe epilepsy.
J Neurosci. 2015; 35: 6600-6618
Dynamic, cell-type-specific roles for GABAergic interneurons in a mouse model of Optogenetically inducible seizures.
Neuron. 2017; 93: 291-298
Convergence and divergence of neurotransmitter action in human cerebral cortex.
Proc Natl Acad Sci U S A. 1989; 86: 8098-8102
Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects.
J Neurosci. 1994; 14: 5485-5502
Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: a dynamic clamp study.
Proc Natl Acad Sci U S A. 1996; 93: 13245-13249
Medial ganglionic eminence progenitors transplanted into hippocampus integrate in a functional and subtype-appropriate manner.
eNeuro. 2017; 4
Human induced pluripotent stem cell-derived MGE cell grafting after status epilepticus attenuates chronic epilepsy and comorbidities via synaptic integration.
Proc Natl Acad Sci U S A. 2019; 116: 287-296
Persistent seizure control in epileptic mice transplanted with gamma-aminobutyric acid progenitors.
Ann Neurol. 2017; 82: 530-542
Transplant of GABAergic precursors restores hippocampal inhibitory function in a mouse model of seizure susceptibility.
Cell Transplant. 2010; 19: 549-564
Transplantation of inhibitory precursor cells from medial ganglionic eminence produces distinct responses in two different models of acute seizure induction.
Epilepsy Behav. 2017; 70: 125-130
Human fetal brain-derived neural stem/progenitor cells grafted into the adult epileptic brain restrain seizures in rat models of temporal lobe epilepsy.
PLoS One. 2014; 9e104092
Cortical GABAergic interneuron/progenitor transplantation as a novel therapy for intractable epilepsy.
Front Cell Neurosci. 2018; 12: 167
Anticonvulsant effects after grafting of rat, porcine, and human mesencephalic neural progenitor cells into the rat subthalamic nucleus.
Exp Neurol. 2018; 310: 70-83
Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain.
J Neurosci. 2006; 26: 7380-7389
Synaptic integration of transplanted interneuron progenitor cells into native cortical networks.
J Neurophysiol. 2016; 116: 472-478
Interneuron transplantation as a treatment for epilepsy.
Cold Spring Harb Perspect Med. 2015; 5
GABA progenitors grafted into the adult epileptic brain control seizures and abnormal behavior.
Nat Neurosci. 2013; 16: 692-697
Bidirectional homeostatic plasticity induced by interneuron cell death and transplantation in vivo.
Proc Natl Acad Sci U S A. 2014; 111: 492-497
Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice.
Proc Natl Acad Sci U S A. 2009; 106: 15472-15477
Grafting of GABAergic precursors rescues deficits in hippocampal inhibition.
Epilepsia. 2010; 51: 66-70
Long-term seizure suppression and optogenetic analyses of synaptic connectivity in epileptic mice with hippocampal grafts of GABAergic interneurons.
J Neurosci. 2014; 34: 13492-13504
Cell therapy using GABAergic neural progenitors.
in: Noebels JL A.M. Rogawski M.A. Olsen R.W. Delgado-Escueta A.V. Source Jasper’s basic mechanisms of the epilepsies. 4th ed. 2012 ([Internet])
Transplantation of GABAergic interneurons into the neonatal primary visual cortex reduces absence seizures in stargazer mice.
Cereb Cortex. 2015; 25: 2970-2979
Comments are closed.