All Title Author
Keywords Abstract


Assortment of GABAergic Plasticity in the Cortical Interneuron Melting Pot

DOI: 10.1155/2011/976856

Full-Text   Cite this paper   Add to My Lib

Abstract:

Cortical structures of the adult mammalian brain are characterized by a spectacular diversity of inhibitory interneurons, which use GABA as neurotransmitter. GABAergic neurotransmission is fundamental for integrating and filtering incoming information and dictating postsynaptic neuronal spike timing, therefore providing a tight temporal code used by each neuron, or ensemble of neurons, to perform sophisticated computational operations. However, the heterogeneity of cortical GABAergic cells is associated to equally diverse properties governing intrinsic excitability as well as strength, dynamic range, spatial extent, anatomical localization, and molecular components of inhibitory synaptic connections that they form with pyramidal neurons. Recent studies showed that similarly to their excitatory (glutamatergic) counterparts, also inhibitory synapses can undergo activity-dependent changes in their strength. Here, some aspects related to plasticity and modulation of adult cortical and hippocampal GABAergic synaptic transmission will be reviewed, aiming at providing a fresh perspective towards the elucidation of the role played by specific cellular elements of cortical microcircuits during both physiological and pathological operations. 1. Introduction The cerebral cortex (which includes the hippocampus, the entorhinal cortex, the piriform cortex, and the neocortex) is the origin of the most sophisticated cognitive functions and complex behaviors. Indeed, the constant computation of incoming sensory information is dynamically integrated to provide a coherent representation of the world, elaborate the past, predict the future, and ultimately develop a consciousness and the self. In particular, the specific activity states of intricate cortical networks often produce a wide range of rhythmic activities, believed to provide the computational substrate for different aspects of cognition and various behaviors [1, 2]. Cortical oscillations range from slow-wave activity (<1?Hz) to ultrafast oscillations (>100?Hz), with several intermediate rhythms (e.g., theta, beta gamma), each of which is considered to underlie specific cognitive aspects, such as non-REM sleep (slow-waves), sensory integration (gamma), working memory (theta), and motor planning (beta) [1]. Importantly, inhibitory neurons were proposed to play a fundamental role in the genesis of most of these rhythms [3–13] through the specialized activity of their GABAergic synapses [7–10]. In fact, it is noteworthy that malfunctioning of specific GABAergic circuits is often indicated as a leading

References

[1]  X. J. Wang, “Neurophysiological and computational principles of cortical rhythms in cognition,” Physiological Reviews, vol. 90, no. 3, pp. 1195–1268, 2010.
[2]  G. Buzsáki and A. Draguhn, “Neuronal olscillations in cortical networks,” Science, vol. 304, no. 5679, pp. 1926–1929, 2004.
[3]  T. Klausberger and P. Somogyi, “Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations,” Science, vol. 321, no. 5885, pp. 53–57, 2008.
[4]  A. Bragin, G. Jando, Z. Nadasdy, J. Hetke, K. Wise, and G. Buzsaki, “Gamma (40–100?Hz) oscillation in the hippocampus of the behaving rat,” Journal of Neuroscience, vol. 15, no. 1, pp. 47–60, 1995.
[5]  V. S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth, “Parvalbumin neurons and gamma rhythms enhance cortical circuit performance,” Nature, vol. 459, no. 7247, pp. 698–702, 2009.
[6]  J. A. Cardin, M. Carlen, K. Meletis et al., “Driving fast-spiking cells induces gamma rhythm and controls sensory responses,” Nature, vol. 459, no. 7247, pp. 663–667, 2009.
[7]  M. Bartos, I. Vida, and P. Jonas, “Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks,” Nature Reviews. Neuroscience, vol. 8, no. 1, pp. 45–56, 2007.
[8]  I. Vida, M. Bartos, and P. Jonas, “Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates,” Neuron, vol. 49, no. 1, pp. 107–117, 2006.
[9]  M. Bartos, I. Vida, M. Frotscher et al., “Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 13222–13227, 2002.
[10]  T. F. Freund and I. Katona, “Perisomatic inhibition,” Neuron, vol. 56, no. 1, pp. 33–42, 2007.
[11]  N. Hájos, J. Pálhalini, E. O. Mann, B. Nèmeth, O. Paulsen, and T. F. Freund, “Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro,” Journal of Neuroscience, vol. 24, no. 41, pp. 9127–9137, 2004.
[12]  P. Somogyi and T. Klausberger, “Defined types of cortical interneurone structure space and spike timing in the hippocampus,” Journal of Physiology, vol. 562, no. 1, pp. 9–26, 2005.
[13]  T. Klausberger, P. J. Magill, L. F. Márton et al., “Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo,” Nature, vol. 421, no. 6925, pp. 844–848, 2003.
[14]  F. M. Benes and S. Berretta, “GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder,” Neuropsychopharmacology, vol. 25, no. 1, pp. 1–27, 2001.
[15]  N. Gogolla, J. J. Leblanc, K. B. Quast, T. Sudhof, M. Fagiolini, and T. K. Hensch, “Common circuit defect of excitatory-inhibitory balance in mouse models of autism,” Journal of Neurodevelopmental Disorders, vol. 1, no. 1, pp. 172–181, 2009.
[16]  E. V. Orekhova, T. A. Stroganova, G. Nygren et al., “Excess of high frequency electroencephalogram oscillations in boys with autism,” Biological Psychiatry, vol. 62, no. 9, pp. 1022–1029, 2007.
[17]  P. Levitt, K. L. Eagleson, and E. M. Powell, “Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders,” Trends in Neurosciences, vol. 27, no. 7, pp. 400–406, 2004.
[18]  D. A. Lewis, T. Hashimoto, and D. W. Volk, “Cortical inhibitory neurons and schizophrenia,” Nature Reviews. Neuroscience, vol. 6, no. 4, pp. 312–324, 2005.
[19]  R. G. Morris, E. Anderson, G. S. Lynch, and M. Baudry, “Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5,” Nature, vol. 319, no. 6056, pp. 774–776, 1986.
[20]  R. C. Malenka, “The long-term potential of LTP,” Nature Reviews. Neuroscience, vol. 4, no. 11, pp. 923–926, 2003.
[21]  T. J. McHugh, K. I. Blum, J. Z. Tsien, S. Tonegawa, and M. A. Wilson, “Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice,” Cell, vol. 87, no. 7, pp. 1339–1349, 1996.
[22]  J. L. Gaiarsa, O. Caillard, and Y. B. Ari, “Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance,” Trends in Neurosciences, vol. 25, no. 11, pp. 564–570, 2002.
[23]  T. F. Freund and G. Buzsaki, “Interneurons of the hippocampus,” Hippocampus, vol. 6, no. 4, pp. 347–470, 1996.
[24]  M. Bartos, I. Vida, M. Frotscher, J. R. Geiger, and P. Jonas, “Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network,” Journal of Neurophysiology, vol. 21, no. 8, pp. 2687–2698, 2001.
[25]  M. Bartos, H. Alle, and I. Vida, “Role of microcircuit structure and input integration in hippocampal interneuron recruitment and plasticity,” Neuropharmacology, vol. 60, no. 5, pp. 730–737, 2010.
[26]  D. M. Kullmann and K. P. Lamsa, “LTP and LTD in cortical GABAergic interneurons: emerging rules and roles,” Neuropharmacology, vol. 60, no. 5, pp. 712–719, 2011.
[27]  D. M. Kullmann and K. P. Lamsa, “Long-term synaptic plasticity in hippocampal interneurons,” Nature Reviews. Neuroscience, vol. 8, no. 9, pp. 687–699, 2007.
[28]  Y. Wang, M. Toledo-Rodriguez, A. Gupta et al., “Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat,” Journal of Physiology, vol. 561, no. 1, pp. 65–90, 2004.
[29]  Y. Wang, A. Gupta, M. Toledo-Rodriguez, C. Z. Wu, and H. Markram, “Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex,” Cerebral Cortex, vol. 12, no. 4, pp. 395–410, 2002.
[30]  S. Hefft and P. Jonas, “Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse,” Nature Neuroscience, vol. 8, pp. 1319–1328, 2005.
[31]  M. I. Daw, L. Tricoire, F. Erdelyi, G. Szabo, and C. J. McBain, “Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent,” The Journal of Neuroscience, vol. 29, no. 36, pp. 11112–11122, 2009.
[32]  G. Maccaferri, J. D. Roberts, P. Szucs, C. A. Cottingham, and P. Somogyi, “Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro,” Nature, vol. 524, no. 6993, pp. 91–116, 2000.
[33]  A. Reyes, R. Lujan, A. Rozov, N. Burnashev, P. Somogyi, and B. Sakmann, “Target-cell-specific facilitation and depression in neocortical circuits,” Nature Neuroscience, vol. 1, no. 4, pp. 279–285, 1998.
[34]  Y. Kawaguchi and Y. Kubota, “Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex,” Neuroscience, vol. 85, no. 3, pp. 677–701, 1998.
[35]  Y Kawaguchi and Y . Kubota, “GABAergic cell subtypes and their synaptic connections in rat frontal cortex,” Cerebral Cortex, vol. 7, no. 6, pp. 476–486, 1997.
[36]  G. A. Ascoli, L. Alonso-Nanclares, S. A. Anderson et al., “Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex,” Nature Reviews. Neuroscience, vol. 9, no. 7, pp. 557–568, 2008.
[37]  H. Markram, M. Toledo-Rodriguez, Y. Wang, A. Gupta, G. Silberberg, and C. Wu, “Interneurons of the neocortical inhibitory system,” Nature Reviews. Neuroscience, vol. 5, no. 10, pp. 793–807, 2004.
[38]  C. J. McBain and A. Fisahn, “Interneurons unbound,” Nature Reviews. Neuroscience, vol. 2, no. 1, pp. 11–23, 2001.
[39]  P. E. Castillo, C. Q. Chiu, and R. C. Carroll, “Long-term plasticity at inhibitory synapses,” Current Opinion in Neurobiology, vol. 21, no. 2, pp. 328–338, 2011.
[40]  S. Marinelli, S. Pacioni, A. Cannich, G. Marsicano, and A. Bacci, “Self-modulation of neocortical pyramidal neurons by endocannabinoids,” Nature Neuroscience, vol. 12, no. 12, pp. 1488–1490, 2009.
[41]  J. DeFelipe and I. Farinas, “The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs,” Progress in Neurobiology, vol. 39, no. 6, pp. 563–607, 1992.
[42]  B. W. Connors and M. J. Gutnick, “Intrinsic firing patterns of diverse neocortical neurons,” Trends in Neurosciences, vol. 13, no. 3, pp. 99–104, 1990.
[43]  J. V. Le Bé, G. Silberberg, Y. Wang, and H. Markram, “Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex,” Cerebral Cortex, vol. 17, no. 9, pp. 2204–2213, 2007.
[44]  D. A. McCormick, B. W. Connors, J. W. Lighthall, and D. A. Prince, “Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex,” Journal of Neurophysiology, vol. 54, no. 4, pp. 782–806, 1985.
[45]  S. P. Brown and S. Hestrin, “Intracortical circuits of pyramidal neurons reflect their long-range axonal targets,” Nature, vol. 457, no. 7233, pp. 1133–1136, 2009.
[46]  N. Spruston, “Pyramidal neurons: dendritic structure and synaptic integration,” Nature Reviews. Neuroscience, vol. 9, no. 3, pp. 206–221, 2008.
[47]  Y. Kubota, N. Shigematsu, F. Karube, et al., “Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons,” Cerebral Cortex. In press.
[48]  R. Douglas, H. Markram, and K. Martin, “Neocortex,” in The Synaptic Organization of the Brain, G. Shepherd, Ed., pp. 499–558, Oxford University Press, New York, NY, USA, 2004.
[49]  A. Bacci, U. Rudolph, J. R. Huguenard, and D. A. Prince, “Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses,” Journal of Neuroscience, vol. 23, no. 29, pp. 9664–9674, 2003.
[50]  M. Beierlein, J. R. Gibson, and B. W. Connors, “Two dynamically distinct inhibitory networks in layer 4 of the neocortex,” Journal of Neurophysiology, vol. 90, no. 5, pp. 2987–3000, 2003.
[51]  F. Karube, Y. Kubota, and Y. Kawaguchi, “Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes,” Journal of Neuroscience, vol. 24, no. 12, pp. 2853–2865, 2004.
[52]  G. Maccaferri, “Stratum oriens horizontal interneurone diversity and hippocampal network dynamics,” Journal of Physiology, vol. 562, no. 1, pp. 73–80, 2005.
[53]  F. Pouille and M. Scanziani, “Routing of spike series by dynamic circuits in the hippocampus,” Nature, vol. 429, no. 6993, pp. 717–723, 2004.
[54]  J. Szabadics, G. Tamás, and I. Soltesz, “Different transmitter transients underlie presynaptic cell type specificity of GABA and GABA, fast,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 37, pp. 14831–14836, 2007.
[55]  M. Capogna, “Neurogliaform cells and other interneurons of stratum lacunosum moleculare gate entorhinal-hippocampal dialogue,” Journal of Physiological, vol. 15, no. 589, pp. 1875–1883, 2010.
[56]  T. Karayannis, D. Elfant, I. Huerta-Ocampo, et al., “Slow GABA transient and receptor desensitization shape synaptic responses evoked by hippocampal neurogliaform cells,” Journal of Neuroscience, vol. 30, no. 29, pp. 9898–9909, 2010.
[57]  S. Olah, G. Komlosi, J. Szabadics, et al., “Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex,” Frontiers in Neural Circuits, vol. 1, article 4, 2007.
[58]  D. Johnston, D. Amaral, et al., “Hippocampus,” in Synaptic Organization of the Brain, G. Shepherd, Ed., Oxford University Press, New York, NY, USA, 2004.
[59]  P. Fuentealba, R. Begum, M. Capogna et al., “Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity,” Neuron, vol. 57, no. 6, pp. 917–929, 2008.
[60]  S. R. Williams and G. J. Stuart, “Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons,” Science, vol. 295, no. 5561, pp. 1907–1910, 2002.
[61]  P. Somogyi, “A specific “axo-axonal” interneuron in the visual cortex of the rat,” Brain Research, vol. 136, no. 2, pp. 345–350, 1977.
[62]  J. Szabadics, C. Varga, G. Molnár, S. Oláh, P. Barzó, and G. Tamás, “Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits,” Science, vol. 311, no. 5758, pp. 233–235, 2006.
[63]  S. Khirug, J. Yamada, R. Afzalov, J. Voipio, L. Khiroug, and K. Kaila, “GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1,” Journal of Neuroscience, vol. 28, no. 18, pp. 4635–4639, 2008.
[64]  A. R. Woodruff, S. A. Anderson, and R Yuste, “The enigmatic function of chandelier cells,” Frontiers in Neuroscience, vol. 4, article 201, 2010.
[65]  L. L. Glickfeld, J. D. Roberts, P. Somogyi, and M. Scanziani, “Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis,” Nature Neuroscience, vol. 12, no. 1, pp. 21–23, 2009.
[66]  J. R. Geiger, J. Lübke, A. Roth, M. Frotscher, and P. Jonas, “Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse,” Neuron, vol. 18, no. 6, pp. 1009–1023, 1997.
[67]  L. Gabernet, S. P. Jadhav, D. E. Feldman, M. Carandini, and M. Scanziani, “Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition,” Neuron, vol. 48, no. 2, pp. 315–327, 2005.
[68]  W. Hartig, K. Brauer, and G. Bruckner, “Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons,” NeuroReport, vol. 3, no. 10, pp. 869–872, 1992.
[69]  N. Berardi, T. Pizzorusso, and L. Maffei, “Extracellular matrix and visual cortical plasticity: freeing the synapse,” Neuron, vol. 44, no. 6, pp. 905–908, 2004.
[70]  T. Pizzorusso, P. Medini, N. Berardi, S. Chierzi, J. W. Fawcett, and L. Maffei, “Reactivation of ocular dominance plasticity in the adult visual cortex,” Science, vol. 298, no. 5596, pp. 1248–1251, 2002.
[71]  N. Gogolla, P. Caroni, A. Lüthi, and C. Herry, “Perineuronal nets protect fear memories from erasure,” Science, vol. 325, no. 5945, pp. 1258–1261, 2009.
[72]  I. Bucurenciu, A. Kulik, B. Schwaller, M. Frotscher, and P. Jonas, “Nanodomain coupling between channels and sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse,” Neuron, vol. 57, no. 4, pp. 536–545, 2008.
[73]  A. Tottene, R. Conti, A. Fabbro et al., “Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice,” Neuron, vol. 61, no. 5, pp. 762–773, 2009.
[74]  J. R. Gibson, M. Belerlein, and B. W. Connors, “Two networks of electrically coupled inhibitory neurons in neocortex,” Nature, vol. 402, no. 6757, pp. 75–79, 1999.
[75]  M. Galarreta and S. Hestrin, “A network of fast-spiking cells in the neocortex connected by electrical synapses,” Nature, vol. 402, no. 6757, pp. 72–75, 1999.
[76]  G. Tamás, E. H. Buhl, A. L?rincz, and P. Somogyi, “Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons,” Nature Neuroscience, vol. 3, no. 4, pp. 366–371, 2000.
[77]  B. W. Connors and M. A. Long, “Electrical synapses in the mammalian brain,” Annual Review of Neuroscience, vol. 27, pp. 393–418, 2004.
[78]  S. Hestrin and M. Galarreta, “Electrical synapses define networks of neocortical GABAergic neurons,” Trends in Neurosciences, vol. 28, no. 6, pp. 304–309, 2005.
[79]  G. Tamás, E. H. Buhl, and P. Somogyi, “Massive autaptic self-innervation of GABAergic neurons in cat visual cortex,” Journal of Neuroscience, vol. 17, no. 16, pp. 6352–6364, 1997.
[80]  W. M. Connelly and G. Lees, “Modulation and function of the autaptic connections of layer V fast spiking interneurons in the rat neocortex,” Journal of Physiological, vol. 588, pp. 2047–2063, 2010.
[81]  A. Bacci, J. R. Huguenard, and D. A. Prince, “Functional autaptic neurotransmission in fast-spiking interneurons: a novel form of feedback inhibition in the neocortex,” Journal of Neuroscience, vol. 23, no. 3, pp. 859–866, 2003.
[82]  F. Manseau, S. Marinelli, P. Mendez, et al., “Desynchronization of neocortical networks by asynchronous release of GABA at autaptic and synaptic vontacts from fast-spiking interneurons,” PLoS Biology, vol. 28, no. 8, 2010.
[83]  A. Bacci and J. R. Huguenard, “Enhancement of spike-timing precision by autaptic transmission in neocortical inhibitory interneurons,” Neuron, vol. 49, no. 1, pp. 119–130, 2006.
[84]  R. I. Wilson, G. Kunos, and R. A. Nicoll, “Presynaptic specificity of endocannabinoid signaling in the hippocampus,” Neuron, vol. 31, no. 3, pp. 453–462, 2001.
[85]  T. F. Freund, I. Katona, and D. Piomelli, “Role of endogenous cannabinoids in synaptic signaling,” Physiological Reviews, vol. 83, no. 3, pp. 1017–1066, 2003.
[86]  V. Chevaleyre and P. E. Castillo, “Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability,” Neuron, vol. 38, no. 3, pp. 461–472, 2003.
[87]  G. Sanacora, R. Gueorguieva, C. N. Epperson et al., “Subtype-specific alterations of γ-aminobutyric acid and glutamate in patients with major depression,” Archives of General Psychiatry, vol. 61, no. 7, pp. 705–713, 2004.
[88]  P. E. Croarkin, A. J. Levinson, and Z. J. Daskalakis, “Evidence for GABAergic inhibitory deficits in major depressive disorder,” Neuroscience and Biobehavioral Reviews, vol. 35, no. 3, pp. 818–825, 2010.
[89]  G. Sanacora, G. F. Mason, D. L. Rothman et al., “Reduced cortical γ-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy,” Archives of General Psychiatry, vol. 56, no. 11, pp. 1043–1047, 1999.
[90]  Y. Ben-Ari and G. L. Holmes, “The multiple facets of γ-aminobutyric acid dysfunction in epilepsy,” Current Opinion in Neurology, vol. 18, no. 2, pp. 141–145, 2005.
[91]  H. T. Chao, H. Chen, R. C. Samaco, et al., “Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes,” Nature, vol. 468, no. 7321, pp. 263–269, 2010.
[92]  M. O. Cunningham, J. Hunt, S. Middleton et al., “Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness,” Journal of Neuroscience, vol. 26, no. 10, pp. 2767–2776, 2006.
[93]  G. P. Reynolds and C. L. Beasley, “GABAergic neuronal subtypes in the human frontal cortex—development and deficits in schizophrenia,” Journal of Chemical Neuroanatomy, vol. 22, no. 1-2, pp. 95–100, 2001.
[94]  K. Nakazawa, V. Zsiros, Z. Jiang, et al., “GABAergic interneuron origin of schizophrenia pathophysiology,” Neuropharmacology. In press.
[95]  P. J. Uhlhaas and W. Singer, “Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology,” Neuron, vol. 52, no. 1, pp. 155–168, 2006.
[96]  P. J. Uhlhaas and W. Singer, “Abnormal neural oscillations and synchrony in schizophrenia,” Nature Reviews. Neuroscience, vol. 11, no. 2, pp. 100–113, 2010.
[97]  V. Varga, A. Losonczy, B. V. Zemelman et al., “Fast synaptic subcortical control of hippocampal circuits,” Science, vol. 326, no. 5951, pp. 449–453, 2009.
[98]  T. F. Freund, A. I. Gulyas, L. Acsady, T. Gorcs, and K. Toth, “Serotonergic control of the hippocampus via local inhibitory interneurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 21, pp. 8501–8505, 1990.
[99]  C. F?ldy, S. Y. Lee, J. Szabadics, A. Neu, and I. Soltesz, “Cell type-specific gating of perisomatic inhibition by cholecystokinin,” Nature Neuroscience, vol. 10, no. 9, pp. 1128–1130, 2007.
[100]  M. V. Puig, A. Watakabe, M. Ushimaru, T. Yamamori, and Y. Kawaguchi, “Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT and 5-HT receptors,” Journal of Neuroscience, vol. 30, no. 6, pp. 2211–2222, 2010.
[101]  L. L. Glickfeld, B. V. Atallah, and M. Scanziani, “Complementary modulation of somatic inhibition by opioids and cannabinoids,” Journal of Neuroscience, vol. 28, no. 8, pp. 1824–1832, 2008.
[102]  W. Hu, M. Zhang, B. Czéh, G. Flügge, and W. Zhang, “Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network,” Neuropsychopharmacology, vol. 35, no. 8, pp. 1693–1707, 2010.
[103]  B. Czeh, M. Simon, M. G. van der Hart, B. Schmelting, M. B. Hesselink, and E. Fuchs, “Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: prevention by treatment with a substance P receptor (NK1) antagonist,” Neuropsychopharmacology, vol. 30, no. 1, pp. 67–79, 2005.
[104]  T. V. P. Bliss and T. Lomo, “Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path,” Journal of Physiology, vol. 232, no. 2, pp. 331–356, 1973.
[105]  T. Ohno-Shosaku, T. Maejima, and M. Kano, “Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals,” Neuron, vol. 29, no. 3, pp. 729–738, 2001.
[106]  M. Kano, T. Ohno-Shosaku, Y. Hashimotodani, M. Uchigashima, and M. Watanabe, “Endocannabinoid-mediated control of synaptic transmission,” Physiological Reviews, vol. 89, no. 1, pp. 309–380, 2009.
[107]  V. Chevaleyre, K. A. Takahashi, and P. E. Castillo, “Endocannabinoid-mediated synaptic plasticity in the CNS,” Annual Review of Neuroscience, vol. 29, pp. 37–76, 2006.
[108]  I. Llano, N. Leresche, and A. Marty, “Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents,” Neuron, vol. 6, no. 4, pp. 565–574, 1991.
[109]  T. A. Pitler and B. E. Alger, “Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells,” Journal of Neuroscience, vol. 12, no. 10, pp. 4122–4132, 1992.
[110]  R. I. Wilson and R. A. Nicoll, “Endogenous cannabinoids mediate retrograde signalling at hippocampal synapsess,” Nature, vol. 410, no. 588, p. 592, 2001.
[111]  B. D. Heifets and P. E. Castillo, “Endocannabinoid signaling and long-term synaptic plasticity,” Annual Review of Physiology, vol. 71, pp. 283–306, 2009.
[112]  R. I. Wilson and R. A. Nicoll, “Endocannabinoid signaling in the brain,” Science, vol. 296, no. 5568, pp. 678–682, 2002.
[113]  A. C. Kreitzer and W. G. Regehr, “Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells,” Neuron, vol. 29, no. 3, pp. 717–727, 2001.
[114]  D. Piomelli, “The molecular logic of endocannabinoid signalling,” Nature Reviews. Neuroscience, vol. 4, no. 11, pp. 873–884, 2003.
[115]  N. Stella, P. Schweitzer, and D. Plomelli, “A second endogenous cannabinoid that modulates long-term potentiation,” Nature, vol. 388, no. 6644, pp. 773–778, 1997.
[116]  V. Di Marzo, A. Fontana, H. Cadas et al., “Formation and inactivation of endogenous cannabinoid anandamide in central neurons,” Nature, vol. 372, no. 6507, pp. 686–691, 1994.
[117]  B. D. Heifets, V. Chevaleyre, and P. E. Castillo, “Interneuron activity controls endocannabinoid-mediated presynaptic plasticity through calcineurin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 29, pp. 10250–10255, 2008.
[118]  V. Chevaleyre, B. D. Heifets, P. S. Kaeser, T. C. Südhof, D. P. Purpura, and P. E. Castillo, “Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α,” Neuron, vol. 54, no. 5, pp. 801–812, 2007.
[119]  T. Harkany, C. Holmgren, W. H?rtig et al., “Endocannabinoid-independent retrograde signaling at inhibitory synapses in layer 2/3 of neocortex: involvement of vesicular glutamate transporter 3,” Journal of Neuroscience, vol. 24, no. 21, pp. 4978–4988, 2004.
[120]  Y. Zilberter, “Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex,” Journal of Physiology, vol. 528, no. 3, pp. 489–496, 2000.
[121]  C. D. Holmgren and Y. Zilberter, “Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells,” Journal of Neuroscience, vol. 21, no. 20, pp. 8270–8277, 2001.
[122]  H. Markram, J. Lübke, M. Frotscher, and B. Sakmann, “Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs,” Science, vol. 275, no. 5297, pp. 213–215, 1997.
[123]  J. C. Magee and D. Johnston, “A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons,” Science, vol. 275, no. 5297, pp. 209–213, 1997.
[124]  Y. Dan and M. M. Poo, “Spike timing-dependent plasticity: from synapse to perception,” Physiological Reviews, vol. 86, no. 3, pp. 1033–1048, 2006.
[125]  J. T. Lu, C. Y. Li, J. P. Zhao, M. M. Poo, and X. H. Zhang, “Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type,” Journal of Neuroscience, vol. 27, no. 36, pp. 9711–9720, 2007.
[126]  M. A. Woodin, K. Ganguly, and M. M. Poo, “Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl-transporter activity,” Neuron, vol. 39, no. 5, pp. 807–820, 2003.
[127]  J. S. Haas, T. Nowotny, and H. D. I. Abarbanel, “Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex,” Journal of Neurophysiology, vol. 96, no. 6, pp. 3305–3313, 2006.
[128]  T. Kurotani, K. Yamada, Y. Yoshimura, M. C. Crair, and Y. Komatsu, “State-dependent bidirectional modification of somatic inhibition in neocortical pyramidal cells,” Neuron, vol. 57, no. 6, pp. 905–916, 2008.
[129]  Y. M. Lu, I. M. Mansuy, E. R. Kandel, and J. Roder, “Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP,” Neuron, vol. 26, no. 1, pp. 197–205, 2000.
[130]  Y. Komatsu and Y. Yoshimura, “Activity-dependent maintenance of long-term potentiation at visual cortical inhibitory synapses,” Journal of Neuroscience, vol. 20, no. 20, pp. 7539–7546, 2000.
[131]  Y. Komatsu, “GABAB receptors, monoamine receptors, and postsynaptic inositol trisphosphate-induced release are involved in the induction of long-term potentiation at visual cortical inhibitory synapses,” Journal of Neuroscience, vol. 16, no. 20, pp. 6342–6352, 1996.
[132]  C. Patenaude, C. A. Chapman, S. Bertrand, P. Congar, and J. C. Lacaille, “GABAB receptor- and metabotropic glutamate receptor-dependent cooperative long-term potentiation of rat hippocampal GABAA synaptic transmission,” Journal of Physiological, vol. 553, pp. 155–167, 2003.
[133]  A. Losonczy, A. A. Biro, and Z. Nusser, “Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 5, pp. 1362–1367, 2004.
[134]  A. Neu, C. Foldy, and I. Soltesz, “Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus,” Journal of Physiology, vol. 578, no. 1, pp. 233–247, 2007.
[135]  J. Louren?o, A. Cannich, M. Carta, F. Coussen, C. Mulle, and G. Marsicano, “Synaptic activation of kainate receptors gates presynaptic CB(1) signaling at GABAergic synapses,” Nature Neuroscience, vol. 13, no. 2, pp. 197–204, 2010.
[136]  C. F?ldy, A. Neu, M. V. Jones, and I. Soltesz, “Presynaptic, activity-dependent modulation of cannabinoid type 1 receptor-mediated inhibition of GABA release,” Journal of Neuroscience, vol. 26, no. 5, pp. 1465–1469, 2006.
[137]  J. Kang, L. Jiang, S. A. Goldman, and M. Nedergaard, “Astrocyte-mediated potentiation of inhibitory synaptic transmission,” Nature Neuroscience, vol. 1, no. 8, pp. 683–692, 1998.
[138]  A. Maffei, K. Nataraj, S. B. Nelson, and G. G. Turrigiano, “Potentiation of cortical inhibition by visual deprivation,” Nature, vol. 443, no. 7107, pp. 81–84, 2006.
[139]  S. Patz, M. J. Wirth, T. Gorba, O. Klostermann, and P. Wahle, “Neuronal activity and neurotrophic factors regulate GAD-65/67 mRNA and protein expression in organotypic cultures of rat visual cortex,” European Journal of Neuroscience, vol. 18, no. 1, pp. 1–12, 2003.
[140]  M. Gierdalski, B. Jablonska, E. Siucinska, E. Lech, A. Skibinska, and M. Kossut, “Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning,” Cerebral Cortex, vol. 11, no. 9, pp. 806–815, 2001.
[141]  H. Asada, Y. Kawamura, K. Maruyama et al., “Cleft palate and decreased brain γ-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 12, pp. 6496–6499, 1997.
[142]  B. Chattopadhyaya, G. Di Cristo, C. Z. Wu et al., “GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex,” Neuron, vol. 54, no. 6, pp. 889–903, 2007.
[143]  Z. J. Huang, G. Di Cristo, and F. Ango, “Development of GABA innervation in the cerebral and cerebellar cortices,” Nature Reviews. Neuroscience, vol. 8, no. 9, pp. 673–686, 2007.
[144]  D. Doischer, J. A. Hosp, Y. Yanagawa et al., “Postnatal differentiation of basket cells from slow to fast signaling devices,” Journal of Neuroscience, vol. 28, no. 48, pp. 12956–12968, 2008.
[145]  P. Jonas, J. Bischofberger, D. Fricker, and R. Miles, “Interneuron diversity series: fast in, fast out—temporal and spatial signal processing in hippocampal interneurons,” Trends in Neurosciences, vol. 27, no. 1, pp. 30–40, 2004.
[146]  L. L. Glickfeld and M. Scanziani, “Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells,” Nature Neuroscience, vol. 9, no. 6, pp. 807–815, 2006.
[147]  P. Li, U. Rudolph, and M. M. Huntsman, “Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 29, pp. 12156–12161, 2009.
[148]  K. D. Micheva and C. Beaulieu, “An anatomical substrate for experience-dependent plasticity of the rat barrel field cortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 25, pp. 11834–11838, 1995.
[149]  Y. Jiao, C. Zhang, Y. Yanagawa, and Q. Q. Sun, “Major effects of sensory experiences on the neocortical inhibitory circuits,” Journal of Neuroscience, vol. 26, no. 34, pp. 8691–8701, 2006.
[150]  A. B. Ali, “Presynaptic inhibition of GABAA receptor-mediated unitary IPSPs by cannabinoid receptors at synapses between CCK-positive interneurons in rat hippocampus,” Journal of Neurophysiology, vol. 98, no. 2, pp. 861–869, 2007.
[151]  D. Robbe, S. M. Montgomery, A. Thome, P. E. Rueda-Orozco, B. L. McNaughton, and G. Buzsaki, “Cannabinoids reveal importance of spike timing coordination in hippocampal function,” Nature Neuroscience, vol. 9, no. 12, pp. 1526–1533, 2006.
[152]  N. Hajos, I. Katona, S. S. Naiem et al., “Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations,” European Journal of Neuroscience, vol. 12, no. 9, pp. 3239–3249, 2000.
[153]  M. Galarreta, F. Erdélyi, G. Szabó, and S. Hestrin, “Cannabinoid sensitivity and synaptic properties of 2 GABAergic networks in the neocortex,” Cerebral Cortex, vol. 18, no. 10, pp. 2296–2305, 2008.
[154]  F. Lemtiri-Chlieh and E. S. Levine, “Lack of Depolarization-induced Suppression of Inhibition (DSI) in layer 2/3 interneurons that receive cannabinoid-sensitive inhibitory inputs,” Journal of Neurophysiology, vol. 98, no. 5, pp. 2517–2524, 2007.
[155]  A. L. Bodor, I. Katona, G. Nyiri et al., “Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types,” Journal of Neuroscience, vol. 25, no. 29, pp. 6845–6856, 2005.
[156]  D. A. Fortin and E. S. Levine, “Differential effects of endocannabinoids on glutamatergic and GABAergic inputs to layer 5 pyramidal neurons,” Cerebral Cortex, vol. 17, no. 1, pp. 163–174, 2007.
[157]  C. Kapfer, L. L. Glickfeld, B. V. Atallah, and M. Scanziani, “Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex,” Nature Neuroscience, vol. 10, no. 6, pp. 743–753, 2007.
[158]  T. K. Berger, R. Perin, G. Silberberg, and H. Markram, “Frequency-dependent disynaptic inhibition in the pyramidal network: a ubiquitous pathway in the developing rat neocortex,” Journal of Physiology, vol. 587, no. 22, pp. 5411–5425, 2009.
[159]  G. Silberberg and H. Markram, “Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells,” Neuron, vol. 53, no. 5, pp. 735–746, 2007.
[160]  M. Murayama, E. Pérez-Garci, T. Nevian, T. Bock, W. Senn, and M. E. Larkum, “Dendritic encoding of sensory stimuli controlled by deep cortical interneurons,” Nature, vol. 457, no. 7233, pp. 1137–1141, 2009.
[161]  P. J. Sj?str?m and M. H?usser, “A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons,” Neuron, vol. 51, no. 2, pp. 227–238, 2006.

Full-Text

comments powered by Disqus