Stability of electrical coupling despite massive developmental changes of intrinsic neuronal physiology

Journal of Neuroscience

Volumn 29, Issue 31, 2009, Pages 9761-9770

  Parker, Philip R L ^a,b   Cruikshank, Scott J ^a   Connors, Barry W ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTRICAL SYNAPSE; GAP JUNCTION; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; THALAMUS NUCLEUS;

ACTION POTENTIALS; AGING; ANIMALS; ANIMALS, NEWBORN; CELL MEMBRANE; ELECTRIC STIMULATION; ELECTRICAL SYNAPSES; GAP JUNCTIONS; MEMBRANE POTENTIALS; MICE; NEURONS; PATCH-CLAMP TECHNIQUES; THALAMUS;

EID: 68549113187     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4568-08.2009     Document Type: Article

References (57)

1. Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365-379.
2. Altman J, Bayer SA (1988) Development of the rat thalamus: III. Time and site of origin and settling pattern of neurons of the reticular nucleus. J Comp Neurol 275:406-428.
3. Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, Connors BW, Golomb D (2002) The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J Neurosci 22:4142-4152.
4. Arumugam H, Liu X, Colombo PJ, Corriveau RA, Belousov AB (2005) NMDA receptors regulate developmental gap junction uncoupling via CREB signaling. Nat Neurosci 8:1720-1726.
5. Bennett MV (1966) Physiology of electrotonic junctions. Ann N Y Acad Sci 137:509-539.
6. Blethyn KL, Hughes SW, Crunelli V (2008) Evidence for electrical synapses between neurons of the nucleus reticularis thalami in the adult brain in vitro. Thalamus Relat Syst 4:13-20.
7. Bruzzone R, Dermietzel R (2006) Structure and function of gap junctions in the developing brain. Cell Tissue Res 326:239-248.
8. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G (2003) Selective impairment of hippocampal gamma oscillations in connexin-36 knockout mouse in vivo. J Neurosci 23:1013-1018.
9. Cachope R, Mackie K, Triller A, O'Brien J, Pereda AE (2007) Potentiation of electrical and chemical synaptic transmission mediated by endocannabinoids. Neuron 56:1034-1047.
10. Condorelli DF, Parenti R, Spinella F, Salinaro AT, Belluardo N, Cardile V, Cicirata F (1998) Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur J Neurosci 10:1202-1208.
11. Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
12. Connors BW, Benardo LS, Prince DA (1983) Coupling between neurons of the developing rat neocortex. J Neurosci 3:773-782.
13. Crabtree JW (1996) Organization in the somatosensory sector of the cat's thalamic reticular nucleus. J Comp Neurol 366:207-222.
14. De Biasi S, Amadeo A, Arcelli P, Frassoni C, Spreafico R (1997) Postnatal development of GABA-immunoreactive terminals in the reticular and ventrobasal nuclei of the rat thalamus: a light and electron microscopic study. Neuroscience 76:503-515.
15. Deleuze C, Huguenard JR (2006) Distinct electrical and chemical connectivity maps in the thalamic reticular nucleus: potential roles in synchronization and sensation. J Neurosci 26:8633-8645.
16. Deschênes M, Madariaga-Domich A, Steriade M (1985) Dendrodendritic synapses in the cat reticularis thalami nucleus: a structural basis for thalamic spindle synchronization. Brain Res 334:165-168.
17. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ (2006) Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439:79-83.
18. Elias LA, Kriegstein AR (2008) Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci 31:243-250.
19. Elias LA, Wang DD, Kriegstein AR (2007) Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448:901-907.
20. Fuentealba P, Steriade M (2005) The reticular nucleus revisited: intrinsic and network properties of a thalamic pacemaker. Prog Neurobiol 75:125-141.
21. Fuentealba P, Crochet S, Timofeev I, Bazhenov M, Sejnowski TJ, Steriade M (2004) Experimental evidence and modeling studies support a synchronizing role for electrical coupling in the cat thalamic reticular neurons in vivo. Eur J Neurosci 20:111-119.
22. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
23. Galarreta M, Hestrin S (2002) Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci U S A 99:12438-12443.
24. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
25. Gibson JR, Beierlein M, Connors BW (2005) Functional properties of electrical synapses between inhibitory interneurons of neocortical layer 4. J Neurophysiol 93:467-480.
26. Hanganu IL, Okabe A, Lessmann V, Luhmann HJ (2009) Cellular mechanisms of subplate-driven and cholinergic input-dependent network activity in the neonatal rat somatosensory cortex. Cereb Cortex 19:89-105.
27. Huguenard JR, McCormick DA (2007) Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci 30:350-356.
28. Huguenard JR, Prince DA (1992) A novel T-type current underlies prolonged Ca(2+)-dependent burst firing in GABAergic neurons of rat thalamic reticular nucleus. J Neurosci 12:3804-3817.
29. Jahnsen H, Llinas R (1984) Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol 349:205-226.
30. Jouvet-Mounier D, Astic L, Lacote D (1970) Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol 2:216-239.
31. Kandler K, Katz LC (1995) Neuronal coupling and uncoupling in the developing nervous system. Curr Opin Neurobiol 5:98-105.
32. Khazipov R, Luhmann HJ (2006) Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 29:414-418.
33. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758-761.
34. Lam YW, Nelson CS, Sherman SM (2006) Mapping of the functional interconnections between thalamic reticular neurons using photostimulation. J Neurophysiol 96:2593-2600.
35. Landisman CE, Connors BW (2005) Long-term modulation of electrical synapses in the mammalian thalamus. Science 310:1809-1813.
36. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW (2002) Electrical synapses in the thalamic reticular nucleus. J Neurosci 22:1002-1009.
37. Lee SC, Cruikshank SJ, Connors BW (2006) Role of connexin36 in the electrical synapses between relay neurons in young developing thalamus. Soc Neurosci Abstr 32:132.12.
38. Lee SH, Govindaiah G, Cox CL (2007) Heterogeneity of firing properties among rat thalamic reticular nuleus neurons. J Physiol 582:195-208.
39. Liu XB, Jones EG (2003) Fine structural localization of connexin-36 immunoreactivity in mouse cerebral cortex and thalamus. J Comp Neurol 466:457-467.
40. Long MA, Landisman CE, Connors BW (2004) Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J Neurosci 24:341-349.
41. Lo Turco JJ, Kriegstein AR (1991) Clusters of coupled neuroblasts in embryonic neocortex. Science 252:563-566.
42. Mitrofanis J, Baker GE (1993) Development of the thalamic reticular and perireticular nuclei in rats and their relationship to the course of growing corticofugal and corticopetal axons. J Comp Neurol 338:575-587.
43. Montoro RJ, Yuste R (2004) Gap junctions in developing neocortex: a review. Brain Res Brain Res Rev 47:216-226.
44. Moody WJ, Bosma MM (2005) Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev 85:883-941.
45. Moreno AP, Lau AF (2007) Gap junction channel gating modulated through protein phosphorylation. Prog Biophys Mol Bio 94:107-119.
46. Ohara PT (1988) Synaptic organization of the thalamic reticular nucleus. J Electron Microsc Tech 10:283-292.
47. Ortino B, Inverardi F, Morante-Oria J, Fairen A, Frassoni C (2003) Substrates and routes of migration of early generated neurons in the developing rat thalamus. Eur J Neurosci 18:323-332.
48. Pangratz-Fuehrer S, Rudolph U, Huguenard JR (2007) Giant spontaneous depolarizing potentials in the developing thalamic reticular nucleus. J Neurophysiol 97:2364-2372.
49. Pinault D, Smith Y, Deschênes M (1997) Dendrodendritic and axoaxonic synapses in the thalamic reticular nucleus of the adult rat. J Neurosci 17:3215-3233.
50. Roerig B, Feller MB (2000) Neurotransmitters and gap junctions in developing neural circuits. Brain Res Brain Res Rev 32:86-114.
51. Rörig B, Sutor B (1996) Regulation of gap junction coupling in the developing neocortex. Mol Neurobiol 12:225-249.
52. Sanchez-Vives MV, Bal T, McCormick DA (1997) Inhibitory interactions between perigeniculate GABAergic neurons. J Neurosci 17:8894-8908.
53. Spitzer NC, Ribera AB (1998) Development of electrical excitability in embryonic neurons: mechanisms and roles. J Neurobiol 37:190-197.
54. Warren RA, Jones EG (1997) Maturation of neuronal form and function in a mouse thalamo-cortical circuit. J Neurosci 17:277-295.
55. Warren RA, Agmon A, Jones EG (1994) Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro. J Neurophysiol 72:1993-2003.
56. Yuste R, Peinado A, Katz LC (1992) Neuronal domains in developing neocortex. Science 257:665-669.
57. Zsiros V, Maccaferri G (2008) Noradrenergic modulation of electrical coupling in GABAergic networks of the hippocampus. J Neurosci 28:1804-1815.