Long-term potentiation of excitatory synapses on neocortical somatostatin-expressing interneurons

Journal of Neurophysiology

Volumn 102, Issue 6, 2009, Pages 3251-3259

  Chen, Huan Xin ^a   Jiang, Mali ^a   Akakin, Dilek ^a   Roper, Steven N ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CALCIUM CHANNEL L TYPE; CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FORSKOLIN; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NIMODIPINE; SOMATOSTATIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; INTERNEURON; LONG TERM POTENTIATION; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; THETA RHYTHM;

ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; INTERNEURONS; LONG-TERM POTENTIATION; MICE; MICE, TRANSGENIC; NEOCORTEX; PATCH-CLAMP TECHNIQUES; PICROTOXIN; QUINOXALINES; SOMATOSTATIN; SYNAPSES;

EID: 72749087507     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00641.2009     Document Type: Article

References (57)

1. Alle H, Jonas P, Geiger JR. PTP and LTP at a hippocampal mossy fiber-interneuron synapse. Proc Natl Acad Sci USA 98: 14708-14713, 2001. (Pubitemid 33121456)
2. Aroniadou VA, Teyler TJ. Induction of NMDA receptor-independent longterm potentiation (LTP) in visual cortex of adult rats. Brain Res 584: 169-173, 1992.
3. Bauer EP, LeDoux JE. Heterosynaptic long-term potentiation of inhibitory interneurons in the lateral amygdala. J Neurosci 24: 9507-9512, 2004. (Pubitemid 39441504)
4. Bear MF. A synaptic basis for memory storage in the cerebral cortex. Proc Natl Acad Sci USA 93: 13453-13459, 1996.
5. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003. (Pubitemid 37430000)
6. Buzsáki G, Geisler C, Henze DA, Wang XJ. Interneuron diversity series: circuit complexity and axon wiring economy of cortical interneurons. Trends Neurosci 27: 186-193, 2004. (Pubitemid 38376405)
7. Castro-Alamancos MA, Calcagnotto ME. Pre-synaptic long-term potentiation in corticothalamic synapses. J Neurosci 19: 9090-9097, 1999.
8. Castro-Alamancos MA, Connors BW. Short-term synaptic enhancement and long-term potentiation in neocortex. Proc Natl Acad Sci USA 93: 1335-1339, 1996. (Pubitemid 26052890)
9. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17: 3894-3906, 1997. (Pubitemid 27200611)
10. Chavez-Noriega LE, Stevens CF. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci 14: 310-317, 1994.
11. Chen HX, Otmakhov N, Strack S, Colbran RJ, Lisman JE. Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? J Neurophysiol 85: 1368-1376, 2001. (Pubitemid 32280578)
12. Christie BR, Franks KM, Seamans JK, Saga K, Sejnowski TJ. Synaptic plasticity in morphologically identified CA1 stratum radiatum interneurons and giant projection cells. Hippocampus 10: 673-683, 2000. (Pubitemid 32045821)
13. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben-Ari Y, Esclapez M, Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4: 52-62, 2001. (Pubitemid 32095526)
14. Degenetais E, Thierry AM, Glowinski J, Gioanni Y. Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex 12: 1-16, 2002. (Pubitemid 33152013)
15. Di Cristo G, Wu C, Chattopadhyaya B, Ango F, Knott G, Welker E, Svoboda K, Huang ZJ. Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci 7: 1184-1186, 2004. (Pubitemid 39426235)
16. 2+ dynamics. J Physiol 551: 67-78, 2003.
17. Halabisky B, Shen F, Huguenard JR, Prince DA. Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 96: 834-845, 2006. (Pubitemid 44155221)
18. Kaiser KM, Lübke J, Zilberter Y, Sakmann B. Postsynaptic calcium influx at single synaptic contacts between pyramidal neurons and bitufted interneurons in layer 2/3 of rat neocortex is enhanced by backpropagating action potentials. J Neurosci 24: 1319-1329, 2004. (Pubitemid 38222982)
19. Kawaguchi Y, Kubota Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387-396, 1993. (Pubitemid 23220322)
20. Kirkwood A, Bear MF. Hebbian synapses in visual cortex. J Neurosci 14: 1634-1645, 1994.
21. Koester HJ, Johnston D. Target cell-dependent normalization of transmitter release at neocortical synapses. Science 308: 863-866, 2005. (Pubitemid 40629268)
22. Kubota Y, Kawaguchi Y. Dependence of GABAergic synaptic areas on the interneuron type and target size. J Neurosci 20: 375-386, 2000. (Pubitemid 30220524)
23. Kullmann DM, Lamsa KP. Long-term synaptic plasticity in hippocampal interneurons. Nat Rev Neurosci 8: 687-699, 2007. (Pubitemid 47283146)
24. Laezza F, Doherty JJ, Dingledine R. Long-term depression in hippocampal interneurons: joint requirement for pre- and post-synaptic events. Science 285: 1411-1414, 1999. (Pubitemid 29411675)
25. Lamsa K, Heeroma JH, Kullmann DM. Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination. Nat Neurosci 8: 916-924, 2005.
26. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA, Kullmann DM. Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315: 1262-1266, 2007. (Pubitemid 46364261)
27. Linden DJ, Ahn S. Activation of pre-synaptic cAMP-dependent protein kinase is required for induction of cerebellar long-term potentiation. J Neurosci 19: 10221-10227, 1999. (Pubitemid 30228029)
28. Lisman JE. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43, 1997.
29. Lu JT, Li CY, Zhao JP, Poo MM, Zhang XH. Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. J Neurosci 27: 9711-9720, 2007.
30. Maccaferri G, McBain CJ. Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16: 5334-5343, 1996. (Pubitemid 26277862)
31. Maccaferri G, Toth K, McBain CJ. Target-specific expression of presynaptic mossy fiber plasticity. Science 279: 1368-1370, 1998. (Pubitemid 28119581)
32. Mahanty NK, Sah P. Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394: 683-687, 1998. (Pubitemid 28389795)
33. Malinow R, Schulman H, Tsien RW. Inhibition of post-synaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245: 862-866, 1989. (Pubitemid 19223665)
34. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
35. Markram H, Wang Y, Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95: 5323-5328, 1998. (Pubitemid 28208596)
36. McMahon LL, Kauer JA. Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18: 295-305, 1997. (Pubitemid 27111111)
37. Mellor J, Nicoll RA. Hippocampal mossy fiber LTP is independent of post-synaptic calcium. Nat Neurosci 4: 125-126, 2001. (Pubitemid 32125254)
38. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16: 815-823, 1996. (Pubitemid 26124058)
39. Mott DD, Dingledine R. Interneuron diversity series: interneuron research - challenges and strategies. Trends Neurosci 26: 484-488, 2003. (Pubitemid 37025786)
40. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20: 3354-3368, 2000. (Pubitemid 30263151)
41. Oliva AA Jr, Lam TT, Swann JW. Distally directed dendrotoxicity induced by kainic acid in hippocampal interneurons of green fluorescent protein-expressing transgenic mice. J Neurosci 22: 8052-8062, 2002.
42. Oren I, Nissen W, Kullmann DM, Somogyi P, Lamsa KP. Role of ionotropic glutamate receptors in long-term potentiation in rat hippocampal CA1 oriens-lacunosum moleculare interneurons. J Neurosci 29: 939-950, 2009.
43. Otmakhov N, Griffith LC, Lisman JE. Post-synaptic inhibitors of calcium/ calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 17: 5357-5365, 1997. (Pubitemid 27300303)
44. Pelkey KA, Lavezzari G, Racca C, Roche KW, McBain CJ. mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 46: 89-102, 2005. (Pubitemid 40488314)
45. Perez Y, Morin F, Lacaille JC. A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci USA 98: 9401-9406, 2001. (Pubitemid 32743929)
46. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285, 1998. (Pubitemid 128712317)
47. Rioult-Pedotti MS, Friedman D, Donoghue JP. Learning-induced LTP in neocortex. Science 290: 533-536, 2000.
48. Salin PA, Malenka RC, Nicoll RA. Cyclic AMP mediates a pre-synaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16: 797-803, 1996.
49. Sarihi A, Jiang B, Komaki A, Sohya K, Yanagawa Y, Tsumoto T. Metabotropic glutamate receptor type 5-dependent long-term potentiation of excitatory synapses on fast-spiking GABAergic neurons in mouse visual cortex. J Neurosci 28: 1224-1235, 2008. (Pubitemid 351186345)
50. 2+ signaling pathway in GABAergic neurons of the hippocampus. Proc Natl Acad Sci USA 95: 3245-3250, 1998.
51. Sloviter RS. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235: 73-76, 1987.
52. Somogyi P, Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562: 9-26, 2005. (Pubitemid 40207780)
53. Sutor B, Hablitz JJ. Long-term potentiation in frontal cortex: role of NMDA-modulated polysynaptic excitatory pathways. Neurosci Lett 97: 111-117, 1989. (Pubitemid 19048920)
54. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265: 1878-1882, 1994.
55. Xia ZG, Refsdal CD, Merchant KM, Dorsa DM, Storm DR. Distribution of mRNA for the calmodulin-sensitive adenylate cyclase in rat brain: expression in areas associated with learning and memory. Neuron 6: 431-443, 1991.
56. Yeckel MF, Kapur A, Johnston D. Multiple forms of LTP in hippocampal CA3 neuronos use a common post-synaptic mechanism. Nat Neurosci 2: 625-633, 1999. (Pubitemid 30491213)
57. Zalutsky RA, Nicoll RA. Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248: 1619-1624, 1990. (Pubitemid 20220133)