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Critical Reviews™ in Neurobiology

年間 3 号発行

ISSN 印刷: 0892-0915

ISSN オンライン: 2375-0014

SJR: 0.121

Role of Giant Depolarizing Potentials in Shaping Synaptic Currents in the Developing Hippocampus

巻 18, 発行 1-2, 2006, pp. 13-23
DOI: 10.1615/CritRevNeurobiol.v18.i1-2.30
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要約

Early in development, network activity in the hippocampus is characterized by giant depolarizing potentials (GDPs). These potentials consist of recurrent membrane depolarizations with superimposed fast action potentials separated by quiescent intervals. They are generated by the interplay of glutamate and γ-aminobutyric acid (GABA) that, in the immediate postnatal period, is depolarizing and excitatory. Here, we review some recent data concerning the functional role of GDPs in shaping synaptic currents at low-probability mossy-fiber (MF)-CA3 synapses. A pairing procedure was used to correlate GDPs-associated calcium increase in the postsynaptic cell with stimulation of afferent inputs. The pairing protocol caused the appearance of synaptic responses or persistently enhanced the number of successes in "presynap-tically" silent or low-probability synapses, respectively. In double-pulses experiments, this effect was associated with a significant reduction in the paired-pulse ratio and a significant increase in the inverse squared value of the coefficient of variation of response amplitude, suggesting that long-term potentiation (LTP) expression was due to the increased probability of transmitter released. In the absence of pairing, no significant changes in synaptic efficacy could be detected. When the interval between GDPs and MF stimulation was increased, the potentiating effect progressively declined and reached the control level in less than 4 s. Mossy-fiber responses were identified on the basis of their paired-pulse facilitation, short-term frequency facilitation, and sensitivity to the group III metabotropic glutamate receptor (mGluR) agonist, 2-amino-4-phosphonobutyric acid (L-AP4). Using these criteria, we found that MFs release mainly GAB A onto CA3 pyramidal cells or GABAergic interneurons. In line with their GABAergic nature, MF responses were blocked by the GABAA receptor antagonists bicuculline or gabazine and were potentiated by NO-711, a blocker of the GABA transporter GAT-1, and by flurazepam, an al-losteric modulator of GABAA receptors. In addition, chemical stimulation of granule cell den-drites with glutamate in the presence of 6,7-dinitroquinoxaline-2,3-dione (DNQX) induced into target neurons barrages of L-AP4-sensitive GABAA-mediated postsynaptic currents, further supporting the GABAergic phenotype of granule cells. As in MF, pairing GDPs with Schaffer collateral stimulation induced a persistent potentiation of spontaneous and evoked α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA)-mediated responses at poorly developed CA3-CA1 synapses. This effect was mediated by an increase in calcium in the postsynaptic cell via voltage-dependent calcium channels activated by the depolarizing action of GABA during GDPs. We provide evidence also that, at these connections, cyclic AMP-dependent protein kinase A (PKA) is the signaling molecule necessary for enhancing synaptic efficacy, since GDPs-induced potentiation was prevented by the membrane permeable PKA inhibitor (PKI 14-22) applied in the bath or by the membrane impermeable form of PKI (PKI 6-22) applied via the patch pipette. In conclusion, it is suggested that GDPs translate specific patterns of pre- and postsynaptic activity into long-lasting changes in synaptic strength and stabilize synaptic connections, thus contributing to the structural refinement of the hippocampal circuit.

によって引用された
  1. Everett Julie C., Licón-Muñoz Yamhilette, Valenzuela C. Fernando, Effects of third trimester-equivalent ethanol exposure on Cl− co-transporter expression, network activity, and GABAergic transmission in the CA3 hippocampal region of neonatal rats, Alcohol, 46, 6, 2012. Crossref

  2. Stafstrom Carl E., Rho Jong M., Neurophysiology of Seizures and Epilepsy, in Swaiman's Pediatric Neurology, 2012. Crossref

  3. Valeeva G. R., Khazipov R. N., Nikolsky E. E., Excitatory Effects of GABA during Ontogeny, Neuroscience and Behavioral Physiology, 43, 5, 2013. Crossref

  4. Cserep C., Szonyi A., Veres J. M., Nemeth B., Szabadits E., de Vente J., Hajos N., Freund T. F., Nyiri G., Nitric Oxide Signaling Modulates Synaptic Transmission during Early Postnatal Development, Cerebral Cortex, 21, 9, 2011. Crossref

  5. Ben-Ari Y., GABA, in Cellular Migration and Formation of Neuronal Connections, 2013. Crossref

  6. Rho Jong M., Another Look at Early GABAergic Neurotransmission: Maybe It's Not So Exciting after All!, Epilepsy Currents, 10, 5, 2010. Crossref

  7. Zhu Hong, Zhang Junjian, Sun Huimin, Zhang Lei, Liu Hui, Zeng Xingxing, Yang Ying, Yao Zhaohui, An enriched environment reverses the synaptic plasticity deficit induced by chronic cerebral hypoperfusion, Neuroscience Letters, 502, 2, 2011. Crossref

  8. Guérit Sylvaine, Allain Anne-Emilie, Léon Céline, Cazenave William, Ferrara Napoleone, Branchereau Pascal, Bikfalvi Andréas, VEGF modulates synaptic activity in the developing spinal cord, Developmental Neurobiology, 74, 11, 2014. Crossref

  9. Lemak Maria S., Voloshanenko Oksana, Draguhn Andreas, Egorov Alexei V., KATP channels modulate intrinsic firing activity of immature entorhinal cortex layer III neurons, Frontiers in Cellular Neuroscience, 8, 2014. Crossref

  10. Holmgren Carl D., Mukhtarov Marat, Malkov Anton E., Popova Irina Y., Bregestovski Piotr, Zilberter Yuri, Energy substrate availability as a determinant of neuronal resting potential, GABA signaling and spontaneous network activity in the neonatal cortexin vitro, Journal of Neurochemistry, 112, 4, 2010. Crossref

  11. Kulagina I. B., Kaspirzhny A. V., Korogod S. M., Organization of Activity of Hippocampal Pyramidal Neurons under Coactivation of Dendritic Glutamate- and GABA-Sensitive Receptors: a Simulation Study, Neurophysiology, 46, 2, 2014. Crossref

  12. Blankenship Aaron G., Ford Kevin J., Johnson Juliette, Seal Rebecca P., Edwards Robert H., Copenhagen David R., Feller Marla B., Synaptic and Extrasynaptic Factors Governing Glutamatergic Retinal Waves, Neuron, 62, 2, 2009. Crossref

  13. Blankenship Aaron G., Feller Marla B., Mechanisms underlying spontaneous patterned activity in developing neural circuits, Nature Reviews Neuroscience, 11, 1, 2010. Crossref

  14. Verwilst Peter, Sunwoo Kyoung, Kim Jong Seung, The role of copper ions in pathophysiology and fluorescent sensors for the detection thereof, Chemical Communications, 51, 26, 2015. Crossref

  15. Luo Pan, Lu Yun, Li Changjun, Zhou Mei, Chen Cheng, Lu Qing, Xu Xulin, He Zhi, Guo Lianjun, Long-lasting spatial learning and memory impairments caused by chronic cerebral hypoperfusion associate with a dynamic change of HCN1/HCN2 expression in hippocampal CA1 region, Neurobiology of Learning and Memory, 123, 2015. Crossref

  16. Luo Pan, Zhang Xiaoxue, Lu Yun, Chen Cheng, Li Changjun, Zhou Mei, Lu Qing, Xu Xulin, Shen Guanxin, Guo Lianjun, Fluoxetine ameliorates cognitive impairments induced by chronic cerebral hypoperfusion via down-regulation of HCN2 surface expression in the hippocampal CA1 area in rats, Pharmacology Biochemistry and Behavior, 140, 2016. Crossref

  17. Zhvania Mzia G., Ksovreli Mariam, Japaridze Nadezhda J., Lordkipanidze Tamar G., Ultrastructural changes to rat hippocampus in pentylenetetrazol- and kainic acid-induced status epilepticus: A study using electron microscopy, Micron, 74, 2015. Crossref

  18. Marshall Audrey G., McCarthy Molly M., Brishnehan Kirk M., Rao Venugopal, Batia Lyn M., Gupta Madhul, Das Srijit, Mitra Nilesh K., Chaudhuri Joydeep D., Effect of gestational ethanol exposure on parvalbumin and calretinin expressing hippocampal neurons in a chick model of fetal alcohol syndrome, Alcohol, 43, 2, 2009. Crossref

  19. Dumas Theodore C., Postnatal alterations in induction threshold and expression magnitude of long-term potentiation and long-term depression at hippocampal synapses, Hippocampus, 22, 2, 2012. Crossref

  20. Dehorter N., Vinay L., Hammond C., Ben-Ari Y., Timing of developmental sequences in different brain structures: physiological and pathological implications, European Journal of Neuroscience, 35, 12, 2012. Crossref

  21. Palanisamy A., Maternal anesthesia and fetal neurodevelopment, International Journal of Obstetric Anesthesia, 21, 2, 2012. Crossref

  22. Silvestre de Ferron Benoît, Vilpoux Catherine, Kervern Myriam, Robert Alexandre, Antol Johan, Naassila Mickael, Pierrefiche Olivier, Increase of KCC2 in hippocampal synaptic plasticity disturbances after perinatal ethanol exposure, Addiction Biology, 22, 6, 2017. Crossref

  23. McVea David A., Murphy Timothy H., Mohajerani Majid H., Large Scale Cortical Functional Networks Associated with Slow-Wave and Spindle-Burst-Related Spontaneous Activity, Frontiers in Neural Circuits, 10, 2016. Crossref

  24. Cserép Csaba, Szabadits Eszter, Szőnyi András, Watanabe Masahiko, Freund Tamás F., Nyiri Gábor, Tell Fabien, NMDA Receptors in GABAergic Synapses during Postnatal Development, PLoS ONE, 7, 5, 2012. Crossref

  25. Morton Russell A., Valenzuela C. Fernando, Third Trimester Equivalent Alcohol Exposure Reduces Modulation of Glutamatergic Synaptic Transmission by 5-HT1A Receptors in the Rat Hippocampal CA3 Region, Frontiers in Neuroscience, 10, 2016. Crossref

  26. Ito Susumu, GABA and glycine in the developing brain, The Journal of Physiological Sciences, 66, 5, 2016. Crossref

  27. Khalilov Ilgam, Minlebaev Marat, Mukhtarov Marat, Juzekaeva Elvira, Khazipov Roustem, Postsynaptic GABA(B) Receptors Contribute to the Termination of Giant Depolarizing Potentials in CA3 Neonatal Rat Hippocampus, Frontiers in Cellular Neuroscience, 11, 2017. Crossref

  28. Ehrlich David E., Ryan Steven J., Hazra Rimi, Guo Ji-Dong, Rainnie Donald G., Postnatal maturation of GABAergic transmission in the rat basolateral amygdala, Journal of Neurophysiology, 110, 4, 2013. Crossref

  29. Ben-Ari Yehezkel, Khalilov Ilgam, Kahle Kristopher T., Cherubini Enrico, The GABA Excitatory/Inhibitory Shift in Brain Maturation and Neurological Disorders, The Neuroscientist, 18, 5, 2012. Crossref

  30. Chung Beryl Y.T., Bailey Craig D.C., Similar nicotinic excitability responses across the developing hippocampal formation are regulated by small-conductance calcium-activated potassium channels, Journal of Neurophysiology, 119, 5, 2018. Crossref

  31. Chung Beryl Y.T., Bailey Craig D.C., Sex differences in the nicotinic excitation of principal neurons within the developing hippocampal formation, Developmental Neurobiology, 2018. Crossref

  32. Wei Kai, Chen Ping, Shen Feng-Yan, Zhang Yu, Liu Yi-Heng, Wang Zhi-Ru, Loepke Andreas W., Wang Ying-Wei, Deng Meng, Defining the Vulnerability Window of Anesthesia-Induced Neuroapoptosis in Developing Dentate Gyrus Granule Cells — A Transgenic Approach Utilizing POMC-EGFP Mice, Neuroscience, 415, 2019. Crossref

  33. Sipilä Sampsa T., Kaila Kai K., GABAergic Transmission and Neuronal Network Events During Hippocampal Development, in Developmental Plasticity of Inhibitory Circuitry, 2010. Crossref

  34. Wang Chang-Zheng, Ma Jian, Xu Ye-Qian, Jiang Shao-Na, Chen Tian-Qi, Yuan Zu-Liang, Mao Xiao-Yi, Zhang Shu-Qing, Liu Lin-Yun, Fu Yinghui, Yu Yong-Chun, Early-generated interneurons regulate neuronal circuit formation during early postnatal development, eLife, 8, 2019. Crossref

  35. Ben-Ari Yehezkel, The GABA developmental shift in health and disease, in Synapse Development and Maturation, 2020. Crossref

  36. Forro Csaba, Caron Davide, Angotzi Gian, Gallo Vincenzo, Berdondini Luca, Santoro Francesca, Palazzolo Gemma, Panuccio Gabriella, Electrophysiology Read-Out Tools for Brain-on-Chip Biotechnology, Micromachines, 12, 2, 2021. Crossref

  37. Maguire Jamie L., Same Channel, Different Tune, Epilepsy Currents, 21, 2, 2021. Crossref

  38. Lopatynska-Mazurek Malgorzata, Komsta Lukasz, Gibula-Tarlowska Ewa, Kotlinska Jolanta H., Aversive Learning Deficits and Depressive-Like Behaviors Are Accompanied by an Increase in Oxidative Stress in a Rat Model of Fetal Alcohol Spectrum Disorders: The Protective Effect of Rapamycin, International Journal of Molecular Sciences, 22, 13, 2021. Crossref

  39. Felix Lisa, Stephan Jonathan, Rose Christine R., Astrocytes of the early postnatal brain, European Journal of Neuroscience, 54, 5, 2021. Crossref

  40. Basu Sudeepta K., Pradhan Subechhya, du Plessis Adre J., Ben-Ari Yehezkel, Limperopoulos Catherine, GABA and glutamate in the preterm neonatal brain: In-vivo measurement by magnetic resonance spectroscopy, NeuroImage, 238, 2021. Crossref

  41. Mayer Margot, Arrizabalaga Onetsine, Ciba Manuel, Schroeder Insa S., Ritter Sylvia, Thielemann Christiane, Novel in vitro assay to investigate radiation induced changes in the functionality of human embryonic stem cell-derived neurospheres, NeuroToxicology, 79, 2020. Crossref

  42. Melzer Sarah, Monyer Hannah, Diversity and function of corticopetal and corticofugal GABAergic projection neurons, Nature Reviews Neuroscience, 21, 9, 2020. Crossref

  43. Dodani Sheel C., Firl Alana, Chan Jefferson, Nam Christine I., Aron Allegra T., Onak Carl S., Ramos-Torres Karla M., Paek Jaeho, Webster Corey M., Feller Marla B., Chang Christopher J., Copper is an endogenous modulator of neural circuit spontaneous activity, Proceedings of the National Academy of Sciences, 111, 46, 2014. Crossref

  44. Moore Anna R., Zhou Wen-Liang, Sirois Carissa L., Belinsky Glenn S., Zecevic Nada, Antic Srdjan D., Connexin hemichannels contribute to spontaneous electrical activity in the human fetal cortex, Proceedings of the National Academy of Sciences, 111, 37, 2014. Crossref

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