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  1. Article: Electrical Coupling between Parvalbumin Basket Cells is Reduced after Experimental Status Epilepticus.

    Yu, Jiandong / Santhakumar, Vijayalakshmi

    bioRxiv : the preprint server for biology

    2023  

    Abstract: Acquired epilepsies, characterized by abnormal increase in hypersynchronous network activity, can be precipitated by various factors including brain injuries which cause neuronal loss and increases in network excitability. Electrical coupling between ... ...

    Abstract Acquired epilepsies, characterized by abnormal increase in hypersynchronous network activity, can be precipitated by various factors including brain injuries which cause neuronal loss and increases in network excitability. Electrical coupling between neurons, mediated by gap junctions, has been shown to enhance synchronous neuronal activity and promote excitotoxic neurodegeneration. Consequently, neuronal gap junctional coupling has been proposed to contribute to development of epilepsy. Parvalbumin expressing interneurons (PV-INs), noted for their roles in powerful perisomatic inhibition and network oscillations, have gap junctions formed exclusively by connexin 36 subunits which show changes in expression following seizures, and in human and experimental epilepsy. However, only a fraction of the connexin hemichannels form functional connections, leaving open the critical question of whether functional gap junctional coupling between neurons is altered during development of epilepsy. Using a pilocarpine induced status epilepticus (SE) model of acquired temporal lobe epilepsy in rat, this study examined changes in electrical coupling between PV-INs in the hippocampal dentate gyrus one week after SE. Contrary to expectations, SE selectively reduced the probability of electrical coupling between PV-INs without altering coupling coefficient. Both coupling frequency and coupling coefficient between non-parvalbumin interneurons remained unchanged after SE. The early and selective decrease in functional electrical coupling between dentate PV-INs after SE may represent a compensatory mechanism to limit excitotoxic damage of fast-spiking interneurons and network synchrony during epileptogenesis.
    Language English
    Publishing date 2023-09-29
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.09.27.559804
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  2. Article: Editorial: Neuroinflammation in acquired epilepsy.

    Jiang, Jianxiong / Santhakumar, Vijayalakshmi / Zhu, Xinjian

    Frontiers in cell and developmental biology

    2022  Volume 10, Page(s) 1074537

    Language English
    Publishing date 2022-11-07
    Publishing country Switzerland
    Document type Editorial
    ZDB-ID 2737824-X
    ISSN 2296-634X
    ISSN 2296-634X
    DOI 10.3389/fcell.2022.1074537
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  3. Article ; Online: Antiepileptogenic and neuroprotective effect of mefloquine after experimental status epilepticus.

    Shao, Mingting / Yu, Hang / Santhakumar, Vijayalakshmi / Yu, Jiandong

    Epilepsy research

    2023  Volume 198, Page(s) 107257

    Abstract: Acquired temporal lobe epilepsy (TLE) characterized by spontaneous recurrent seizures (SRS) and hippocampal inhibitory neuron dysfunction is often refractory to current therapies. Gap junctional or electrical coupling between inhibitory neurons has been ... ...

    Abstract Acquired temporal lobe epilepsy (TLE) characterized by spontaneous recurrent seizures (SRS) and hippocampal inhibitory neuron dysfunction is often refractory to current therapies. Gap junctional or electrical coupling between inhibitory neurons has been proposed to facilitate network synchrony and intercellular molecular exchange suggesting a role in both seizures and neurodegeneration. While gap junction blockers can limit acute seizures, whether blocking neuronal gap junctions can modify development of chronic epilepsy has not been examined. This study examined whether mefloquine, a selective blocker of Connexin 36 gap junctions which are well characterized in inhibitory neurons, can limit epileptogenesis and related cellular and behavioral pathology in a model of acquired TLE. A single, systemic dose of mefloquine administered early after pilocarpine-induced status epilepticus (SE) in rat reduced both development of SRS and behavioral co-morbidities. Immunostaining for interneuron subtypes identified that mefloquine treatment likely reduced delayed inhibitory neuronal loss after SE. Uniquely, parvalbumin expressing neurons in the hippocampal dentate gyrus appeared relatively resistant to early cell loss after SE. Functionally, whole cell patch clamp recordings revealed that mefloquine treatment preserved inhibitory synaptic drive to projection neurons one week and one month after SE. These results demonstrate that mefloquine, a drug already approved for malaria prophylaxis, is potentially antiepileptogenic and can protect against progressive interneuron loss and behavioral co-morbidities of epilepsy.
    MeSH term(s) Rats ; Animals ; Neuroprotective Agents/adverse effects ; Mefloquine/adverse effects ; Status Epilepticus/chemically induced ; Status Epilepticus/drug therapy ; Status Epilepticus/pathology ; Seizures/chemically induced ; Epilepsy, Temporal Lobe ; Hippocampus ; Epilepsy/pathology ; Pilocarpine/toxicity ; Disease Models, Animal
    Chemical Substances Neuroprotective Agents ; Mefloquine (TML814419R) ; Pilocarpine (01MI4Q9DI3)
    Language English
    Publishing date 2023-11-08
    Publishing country Netherlands
    Document type Journal Article
    ZDB-ID 632939-1
    ISSN 1872-6844 ; 0920-1211
    ISSN (online) 1872-6844
    ISSN 0920-1211
    DOI 10.1016/j.eplepsyres.2023.107257
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  4. Article: Current

    Hamilton, Kelly Andrew / Santhakumar, Vijayalakshmi

    Current opinion in biomedical engineering

    2020  Volume 14, Page(s) 18–24

    Abstract: Traumatic brain injury often leads to progressive alterations at the molecular to circuit levels resulting in epilepsy and memory impairments. ...

    Abstract Traumatic brain injury often leads to progressive alterations at the molecular to circuit levels resulting in epilepsy and memory impairments.
    Language English
    Publishing date 2020-05-11
    Publishing country England
    Document type Journal Article
    ISSN 2468-4511
    ISSN 2468-4511
    DOI 10.1016/j.cobme.2020.05.001
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  5. Article ; Online: Editorial

    Jianxiong Jiang / Vijayalakshmi Santhakumar / Xinjian Zhu

    Frontiers in Cell and Developmental Biology, Vol

    Neuroinflammation in acquired epilepsy

    2022  Volume 10

    Keywords epileptogenesis ; BDNF ; biomarker ; brain infection ; NADPH oxidase ; oxidative stress ; Biology (General) ; QH301-705.5
    Language English
    Publishing date 2022-11-01T00:00:00Z
    Publisher Frontiers Media S.A.
    Document type Article ; Online
    Database BASE - Bielefeld Academic Search Engine (life sciences selection)

    Full text online

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  6. Article: Dysregulation of Neuropilin-2 Expression in Inhibitory Neurons Impairs Hippocampal Circuit Development Leading to Autism-Epilepsy Phenotype.

    Subramanian, Deepak / Eisenberg, Carol / Huang, Andrew / Baek, Jiyeon / Naveed, Haniya / Komatireddy, Samiksha / Shiflett, Michael W / Tran, Tracy S / Santhakumar, Vijayalakshmi

    bioRxiv : the preprint server for biology

    2024  

    Abstract: Dysregulation of development, migration, and function of interneurons, collectively termed interneuronopathies, have been proposed as a shared mechanism for autism spectrum disorders (ASDs) and childhood epilepsy. Neuropilin-2 (Nrp2), a candidate ASD ... ...

    Abstract Dysregulation of development, migration, and function of interneurons, collectively termed interneuronopathies, have been proposed as a shared mechanism for autism spectrum disorders (ASDs) and childhood epilepsy. Neuropilin-2 (Nrp2), a candidate ASD gene, is a critical regulator of interneuron migration from the median ganglionic eminence (MGE) to the pallium, including the hippocampus. While clinical studies have identified Nrp2 polymorphisms in patients with ASD, whether dysregulation of Nrp2-dependent interneuron migration contributes to pathogenesis of ASD and epilepsy has not been tested. We tested the hypothesis that the lack of Nrp2 in MGE-derived interneuron precursors disrupts the excitation/inhibition balance in hippocampal circuits, thus predisposing the network to seizures and behavioral patterns associated with ASD. Embryonic deletion of Nrp2 during the developmental period for migration of MGE derived interneuron precursors (iCKO) significantly reduced parvalbumin, neuropeptide Y, and somatostatin positive neurons in the hippocampal CA1. Consequently, when compared to controls, the frequency of inhibitory synaptic currents in CA1 pyramidal cells was reduced while frequency of excitatory synaptic currents was increased in iCKO mice. Although passive and active membrane properties of CA1 pyramidal cells were unchanged, iCKO mice showed enhanced susceptibility to chemically evoked seizures. Moreover, iCKO mice exhibited selective behavioral deficits in both preference for social novelty and goal-directed learning, which are consistent with ASD-like phenotype. Together, our findings show that disruption of developmental Nrp2 regulation of interneuron circuit establishment, produces ASD-like behaviors and enhanced risk for epilepsy. These results support the developmental interneuronopathy hypothesis of ASD epilepsy comorbidity.
    Language English
    Publishing date 2024-02-06
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2024.02.05.578976
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  7. Article ; Online: Traumatic brain injury metabolome and mitochondrial impact after early stage Ru360 treatment.

    Chitturi, Jyothsna / Santhakumar, Vijayalakshmi / Kannurpatti, Sridhar S

    Mitochondrion

    2021  Volume 57, Page(s) 192–204

    Abstract: Ru360, a mitochondrial ... ...

    Abstract Ru360, a mitochondrial Ca
    MeSH term(s) Animals ; Brain Injuries, Traumatic/drug therapy ; Brain Injuries, Traumatic/metabolism ; Brain Injuries, Traumatic/psychology ; Chromatography, Liquid ; Disease Models, Animal ; Energy Metabolism/drug effects ; Glycolysis/drug effects ; Male ; Mass Spectrometry ; Metabolomics/methods ; Mitochondria/metabolism ; Pentose Phosphate Pathway/drug effects ; Rats ; Rats, Sprague-Dawley ; Reactive Oxygen Species/metabolism ; Ruthenium Compounds/administration & dosage ; Ruthenium Compounds/pharmacology
    Chemical Substances Reactive Oxygen Species ; Ru 360 ; Ruthenium Compounds
    Language English
    Publishing date 2021-01-21
    Publishing country Netherlands
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
    ZDB-ID 2056923-3
    ISSN 1872-8278 ; 1567-7249
    ISSN (online) 1872-8278
    ISSN 1567-7249
    DOI 10.1016/j.mito.2021.01.003
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  8. Article: RECLUSIVE CHANDELIERS: FUNCTIONAL ISOLATION OF DENTATE AXO-AXONIC CELLS AFTER EXPERIMENTAL STATUS EPILEPTICUS.

    Proddutur, Archana / Nguyen, Susan / Yeh, Chia-Wei / Gupta, Akshay / Santhakumar, Vijayalakshmi

    bioRxiv : the preprint server for biology

    2023  

    Abstract: Axo-axonic cells (AACs) provide specialized inhibition to the axon initial segment (AIS) of excitatory neurons and can regulate network output and synchrony. Although hippocampal dentate AACs are structurally altered in epilepsy, physiological analyses ... ...

    Abstract Axo-axonic cells (AACs) provide specialized inhibition to the axon initial segment (AIS) of excitatory neurons and can regulate network output and synchrony. Although hippocampal dentate AACs are structurally altered in epilepsy, physiological analyses of dentate AACs are lacking. We demonstrate that parvalbumin neurons in the dentate molecular layer express PTHLH, an AAC marker, and exhibit morphology characteristic of AACs. Dentate AACs show high-frequency, non-adapting firing but lack persistent firing in the absence of input and have higher rheobase than basket cells suggesting that AACs can respond reliably to network activity. Early after pilocarpine-induced status epilepticus (SE), dentate AACs receive fewer spontaneous excitatory and inhibitory synaptic inputs and have significantly lower maximum firing frequency. Paired recordings and spatially localized optogenetic stimulation revealed that SE reduced the amplitude of unitary synaptic inputs from AACs to granule cells without altering reliability, short-term plasticity, or AIS GABA reversal potential. These changes compromised AAC-dependent shunting of granule cell firing in a multicompartmental model. These early post-SE changes in AAC physiology would limit their ability to receive and respond to input, undermining a critical brake on the dentate throughput during epileptogenesis.
    Language English
    Publishing date 2023-10-02
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.10.01.560378
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  9. Article ; Online: Reclusive chandeliers: Functional isolation of dentate axo-axonic cells after experimental status epilepticus.

    Proddutur, Archana / Nguyen, Susan / Yeh, Chia-Wei / Gupta, Akshay / Santhakumar, Vijayalakshmi

    Progress in neurobiology

    2023  Volume 231, Page(s) 102542

    Abstract: Axo-axonic cells (AACs) provide specialized inhibition to the axon initial segment (AIS) of excitatory neurons and can regulate network output and synchrony. Although hippocampal dentate AACs are structurally altered in epilepsy, physiological analyses ... ...

    Abstract Axo-axonic cells (AACs) provide specialized inhibition to the axon initial segment (AIS) of excitatory neurons and can regulate network output and synchrony. Although hippocampal dentate AACs are structurally altered in epilepsy, physiological analyses of dentate AACs are lacking. We demonstrate that parvalbumin neurons in the dentate molecular layer express PTHLH, an AAC marker, and exhibit morphology characteristic of AACs. Dentate AACs show high-frequency, non-adapting firing but lack persistent firing in the absence of input and have higher rheobase than basket cells suggesting that AACs can respond reliably to network activity. Early after pilocarpine-induced status epilepticus (SE), dentate AACs receive fewer spontaneous excitatory and inhibitory synaptic inputs and have significantly lower maximum firing frequency. Paired recordings and spatially localized optogenetic stimulation revealed that SE reduced the amplitude of unitary synaptic inputs from AACs to granule cells without altering reliability, short-term plasticity, or AIS GABA reversal potential. These changes compromised AAC-dependent shunting of granule cell firing in a multicompartmental model. These early post-SE changes in AAC physiology would limit their ability to receive and respond to input, undermining a critical brake on the dentate throughput during epileptogenesis.
    MeSH term(s) Humans ; Reproducibility of Results ; Dentate Gyrus ; Neurons/physiology ; Axons ; Status Epilepticus/chemically induced
    Language English
    Publishing date 2023-10-26
    Publishing country England
    Document type Journal Article
    ZDB-ID 185535-9
    ISSN 1873-5118 ; 0301-0082
    ISSN (online) 1873-5118
    ISSN 0301-0082
    DOI 10.1016/j.pneurobio.2023.102542
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  10. Article ; Online: Differential Activity-Dependent Increase in Synaptic Inhibition and Parvalbumin Interneuron Recruitment in Dentate Granule Cells and Semilunar Granule Cells.

    Afrasiabi, Milad / Gupta, Akshay / Xu, Huaying / Swietek, Bogumila / Santhakumar, Vijayalakshmi

    The Journal of neuroscience : the official journal of the Society for Neuroscience

    2022  Volume 42, Issue 6, Page(s) 1090–1103

    Abstract: Strong inhibitory synaptic gating of dentate gyrus granule cells (GCs), attributed largely to fast-spiking parvalbumin interneurons (PV-INs), is essential to maintain sparse network activity needed for dentate dependent behaviors. However, the ... ...

    Abstract Strong inhibitory synaptic gating of dentate gyrus granule cells (GCs), attributed largely to fast-spiking parvalbumin interneurons (PV-INs), is essential to maintain sparse network activity needed for dentate dependent behaviors. However, the contribution of PV-INs to basal and input-driven sustained synaptic inhibition in GCs and semilunar granule cells (SGCs), a sparse morphologically distinct dentate projection neuron subtype, is currently unknown. In studies conducted in hippocampal slices from mice, we find that although basal IPSCs are more frequent in SGCs and optical activation of PV-INs reliably elicited IPSCs in both GCs and SGCs, optical suppression of PV-INs failed to reduce IPSC frequency in either cell type. Amplitude and kinetics of IPSCs evoked by perforant path (PP) activation were not different between GCs and SGCs. However, the robust increase in sustained polysynaptic IPSCs elicited by paired afferent stimulation was lower in SGCs than in simultaneously recorded GCs. Optical suppression of PV-IN selectively reduced sustained IPSCs in SGCs but not in GCs. These results demonstrate that PV-INs, while contributing minimally to basal synaptic inhibition in both GCs and SGCs in slices, mediate sustained feedback inhibition selectively in SGCs. The temporally selective blunting of activity-driven sustained inhibitory gating of SGCs could support their preferential and persistent recruitment during behavioral tasks.
    MeSH term(s) Animals ; Dentate Gyrus/physiology ; Inhibitory Postsynaptic Potentials/physiology ; Interneurons/physiology ; Mice ; Neural Inhibition/physiology ; Neurons/physiology ; Parvalbumins/metabolism ; Synapses/physiology
    Chemical Substances Parvalbumins
    Language English
    Publishing date 2022-01-03
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 604637-x
    ISSN 1529-2401 ; 0270-6474
    ISSN (online) 1529-2401
    ISSN 0270-6474
    DOI 10.1523/JNEUROSCI.1360-21.2021
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