A novel role of dendritic gap junction and mechanisms underlying its interaction with thalamocortical conductance in fast spiking inhibitory neurons

BMC Neuroscience

Volumn 10, Issue , 2009, Pages 131-

  Sun, Qian Quan ^a  

^a UNIVERSITY OF WYOMING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DENDRITE; EXCITATORY JUNCTION POTENTIAL; GAP JUNCTION; ION CURRENT; MOUSE; NERVE FIBER MEMBRANE CONDUCTANCE; NONHUMAN; SPIKE WAVE; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT;

ACTION POTENTIALS; ANIMALS; CELL SHAPE; CEREBRAL CORTEX; COMPUTER SIMULATION; DENDRITES; GAP JUNCTIONS; GLUTAMATE DECARBOXYLASE; INTERNEURONS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; NEURAL CONDUCTION; NEURAL INHIBITION; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; SYNAPSES; THALAMIC NUCLEI;

EID: 70549098694     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-10-131     Document Type: Article

References (61)

1. Bennett MV. Dynamic patterns of brain cell assemblies. IV. Mixed systems. Interneuronal connectivity. Gap junction ultrastructure. Neurosci Res Program Bull 1974, 12:90-94.
2. Bennett MV, Zheng X, Sogin ML. The connexins and their family tree. Soc Gen Physiol Ser 1994, 49:223-233.
3. Bennett MV, Zukin RS. Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 2004, 41:495-511. 10.1016/S0896-6273(04)00043-1, 14980200.
4. Nelson SB. Temporal Interactions in the Cat Visual-System 3. Pharmacological Studies of Cortical Suppression Suggest A Presynaptic Mechanism. Journal of Neuroscience 1991, 11:369-380.
5. Vidyasagar TR, Pei X, Volgushev M. Multiple mechanisms underlying the orientation selectivity of visual cortical neurones. Trends in Neurosciences 1996, 19:272-277. 10.1016/S0166-2236(96)20027-X, 8799969.
6. Cardin JA, Palmer LA, Contreras D. Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex. J Neurosci 2007, 27:10333-10344. 10.1523/JNEUROSCI.1692-07.2007, 17898205.
7. Pouille F, Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163. 10.1126/science.1060342, 11498596.
8. Swadlow HA, Gusev AG. Receptive-field construction in cortical inhibitory interneurons. Nat Neurosci 2002, 5:403-404. 10.1038/nn847, 11967546.
9. Bruno RM, Simons DJ. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 2002, 22:10966-10975.
10. Wehr M, Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 2003, 426:442-446. 10.1038/nature02116, 14647382.
11. Sillito AM. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol 1975, 250:305-329. 1348363, 1177144.
12. Swadlow HA. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 2003, 13:25-32. 10.1093/cercor/13.1.25, 12466212.
13. Sun QQ, Huguenard JR, Prince DA. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 2006, 26:1219-1230. 10.1523/JNEUROSCI.4727-04.2006, 16436609.
14. Cruikshank SJ, Lewis TJ, Connors BW. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10:462-8.
15. Gibson JR, Beierlein M, Conors BW. Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J Neurophysiol 93:467-80. 10.1152/jn.00520.2004, 15317837.
16. Traub RD, Kopell N, Bibbig A, Buhl EH, Lebeau FE, Whittington MA. Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J Neurosci 2001, 21:9478-9486.
17. Galarreta M, Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci USA 2002, 99:12438-12443. 129463, 12213962, 10.1073/pnas.192159599.
18. Lewis TJ, Rinzel J. Dynamics of spiking neurons connected by both inhibitory and electrical coupling. J Comput Neurosci 2003, 14:283-309. 10.1023/A:1023265027714, 12766429.
19. Pfeuty B, Mato G, Golomb D, Hansel D. Electrical synapses and synchrony: the role of intrinsic currents. J Neurosci 2003, 23:6280-6294.
20. Schneider AR, Lewis TJ, Rinzel. Effects of correlated input and electrical coupling on synchrony in fast-spiking cell networks. Neurocomputing 2006, 69:1125-1129.
21. Nadim F, Golowasch J. Signal transmission between gap-junctionally coupled passive cables is most effective at an optimal diameter. J Neurophysiol 2006, 95:3831-43. 10.1152/jn.00033.2006, 16709724.
22. Saraga F, Ng L, Skinner FK. Distal gap junctions and active dendrites can tune network dynamics. J Neurophysiol 2006, 95:1669-82. 10.1152/jn.00662.2005, 16339003.
23. Gansert J, Golowasch J, Nadim F. Sustained rhythmic activity in gap-junctionally coupled networks of model neurons depends on the diameter of coupled dendrites. J Neurophysiol 2007, 98:3450-60. 2413014, 17913989, 10.1152/jn.00648.2007.
24. Castro-Alamancos MA. Origin of synchronized oscillations induced by neocortical disinhibition in vivo. J Neurosci 2000, 20:9195-9206.
25. Sun QQ, Huguenard JR, Prince DA. Reorganization of barrel circuits leads to thalamically-evoked cortical epileptiform activity. Thalamus & Related Systems 2007, 3(04):261-273.
26. Staiger JF, Zilles K, Freund TF. Distribution of GABAergic elements postsynaptic to ventroposteromedial thalamic projections in layer IV of rat barrel cortex. Eur J Neurosci 1996, 8:2273-2285. 10.1111/j.1460-9568.1996.tb01191.x, 8950092.
27. Simons DJ. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 1978, 41:798-820.
28. Fukuda T, Kosaka T, Singer W, Galuske RA. Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci 2006, 26:3434-3443. 10.1523/JNEUROSCI.4076-05.2006, 16571750.
29. Liu XB, Jones EG. Fine structural localization of connexin-36 immunoreactivity in mouse cerebral cortex and thalamus. J Comp Neurol 2003, 466:457-467. 10.1002/cne.10901, 14566942.
30. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 2003, 467:60-79. 10.1002/cne.10905, 14574680.
31. Hines ML, Carnevale NT. The NEURON simulation environment. Comput 1997, 9:1179-1209.
32. Beierlein M, Gibson JR, Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Neurosci 2000, 3:904-910.
33. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 2003, 90:2987-3000. 10.1152/jn.00283.2003, 12815025.
34. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 1999, 402:75-79. 10.1038/47035, 10573419.
35. Castro-Alamancos MA. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog Neurobiol 2004, 74:213-247. 10.1016/j.pneurobio.2004.09.002, 15556288.
36. Castro-Alamancos MA. Vibrissa myoclonus (rhythmic retractions) driven by resonance of excitatory networks in motor cortex. J Neurophysiol 2006, 96:1691-1698. 10.1152/jn.00454.2006, 16807344.
37. Swadlow HA, Beloozerova IN, Sirota MG. Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J Neurophysiol 1998, 79:567-582.
38. Mainen ZF, Joerges J, Huguenard JR, Sejnowski TJ. A model of spike initiation in neocortical pyramidal neurons. Neuron 1995, 15:1427-1439. 10.1016/0896-6273(95)90020-9, 8845165.
39. Destexhe A. Conductance-based integrate-and-fire models. Neural Comput 1997, 9:503-514. 10.1162/neco.1997.9.3.503, 9097470.
40. Priebe NJ, Ferster D. Mechanisms underlying cross-orientation suppression in cat visual cortex. Nat Neurosci 2006, 9:552-561. 10.1038/nn1660, 16520737.
41. Porter JT, Johnson CK, Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 2001, 21:2699-2710.
42. Brecht M, Sakmann B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol 2002, 543:49-70. 2290465, 12181281, 10.1113/jphysiol.2002.018465.
43. Bruno RM, Sakmann B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 2006, 312:1622-1627. 10.1126/science.1124593, 16778049.
44. Castro-Alamancos MA, Connors BW. Thalamocortical synapses. Prog Neurobiol 1997, 51:581-606. 10.1016/S0301-0082(97)00002-6, 9175158.
45. Simons DJ, Woolsey TA. Functional organization in mouse barrel cortex. Brain Res 1979, 165:327-332. 10.1016/0006-8993(79)90564-X, 421142.
46. Connors BW, Long MA. Electrical synapses in the mammalian brain. Annu Rev Neurosci 2004, 27:393-418. 10.1146/annurev.neuro.26.041002.131128, 15217338.
47. Hestrin S, Galarreta M. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci 2005, 28:304-309. 10.1016/j.tins.2005.04.001, 15927686.
48. Mancilla JG, Lewis TJ, Pinto DJ, Rinzel J, Connors BW. Synchronization of electrically coupled pairs of inhibitory interneurons in neocortex. J Neurosci 2007, 27:2058-2073. 10.1523/JNEUROSCI.2715-06.2007, 17314301.
49. Lewis, Rinzel. Dendritic effects in networks of electrically coupled fast-spiking interneurons. Neurocomputing 2004, 58-60:145-150.
50. Simons DJ. Multi-whisker stimulation and its effects on vibrissa units in rat SmI barrel cortex. Brain Res 1983, 276:178-182. 10.1016/0006-8993(83)90561-9, 6626997.
51. Castro-Alamancos MA. Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J Neurophysiol 2002, 87:946-953.
52. Thomson AM. Molecular frequency filters at central synapses. Prog Neurobiol 2000, 62:159-196. 10.1016/S0301-0082(00)00008-3, 10828382.
53. Migliore M, Hines ML, Shepherd GM. The role of distal dendritic gap junctions in synchronization of mitral cell axonal output. J Comput Neurosci 2005, 18:151-161. 10.1007/s10827-005-6556-1, 15714267.
54. Sun QQ. The missing piece in the 'use it or lose it' puzzle: is inhibition regulated by activity or does it act on its own accord?. Rev Neurosci 2007, 18(3-4):295-310. 2408386, 18019611.
55. Pfeuty B, Mato G, Golomb D, Hansel D. The combined effects of inhibitory and electrical synapses in synchrony. Neural Comput 2005, 17:633-70. 10.1162/0899766053019917, 15802009.
56. Bacci A, Huguenard JR, Prince DA. Functional autaptic neurotransmission in fast-spiking interneurons: a novel form of feedback inhibition in the neocortex. J Neurosci 2003, 23:859-866.
57. Zsiros V, Aradi I, Maccaferri G. Propagation of postsynaptic currents and potentials via GJs in GABAergic networks of the rat hippocampus. J Physiol 2007, 578:527-544. 2075142, 17110410, 10.1113/jphysiol.2006.123463.
58. Xiang Z, Huguenard JR, Prince DA. GABAA receptor-mediated currents in interneurons and pyramidal cells of rat visual cortex. J Physiol 1998, 506(Pt 3):715-730. 2230760, 9503333, 10.1111/j.1469-7793.1998.715bv.x.
59. Jiao Y, Zhang C, Yanagawa Y, Sun QQ. Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci 2006, 26:8691-8701. 10.1523/JNEUROSCI.2478-06.2006, 16928857.
60. Agmon A, Connors BW. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 1991, 41:365-379. 10.1016/0306-4522(91)90333-J, 1870696.
61. Xiang Z, Huguenard JR, Prince DA. Synaptic inhibition of pyramidal cells evoked by different interneuronal subtypes in layer v of rat visual cortex. J Neurophysiol 2002, 88:740-750.