Network architecture of gap junction-coupled neuronal linkage in the striatum

Journal of Neuroscience

Volumn 29, Issue 4, 2009, Pages 1235-1243

  Fukuda, Takaichi ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Connexin36; Electron microscopy; Gap junction; Immunohistochemistry; Parvalbumin; Striatum

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ENKEPHALIN; METHIONINE; PARVALBUMIN;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CAT; CAUDATE NUCLEUS; CORPUS STRIATUM; FEMALE; GAP JUNCTION; INFORMATION PROCESSING; INTERNEURON; MALE; NONHUMAN; PRIORITY JOURNAL; PUTAMEN;

ANIMALS; CATS; CONNEXINS; CORPUS STRIATUM; DENDRITES; ENKEPHALIN, METHIONINE; FEMALE; GAP JUNCTIONS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NERVE NET; NEURONS; PARVALBUMINS;

EID: 59649083220     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4418-08.2009     Document Type: Article

References (50)

1. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Aca Sci U S A 99:13222-13227.
2. Bennett BD, Bolam JP (1994a) Localisation of parvalbumin-immunoreactive structures in primate caudate-putamen. J Comp Neurol 347:340-356.
3. Bennett BD, Bolam JP (1994b) Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat. Neuroscience 62:707-719.
4. Bolam JP, Hanley JJ, Booth PA, Bevan MD (2000) Synaptic organization of the basal ganglia. J Anat 196:527-542.
5. Condorelli DF, Parenti R, Spinella F, Trovato Salinaro A, 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.
6. Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
7. Cowan RL, Wilson CJ, Emson PC, Heizmann CW (1990) Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J Comp Neurol 302:197-205.
8. Dermietzel R, Hertberg EL, Kessler JA, Spray DC (1991) Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis. J Neurosci 11:1421-1432.
9. Fukuda T (2007) Structural organization of the gap junction network in the cerebral cortex. Neuroscientist 13:199-207.
10. Fukuda T, Kosaka T (2000) Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 20:1519-1528.
11. Fukuda T, Kosaka T (2003) Ultrastructural study of gap junctions between dendrites of parvalbumin-containing GABAergic neurons in various neocortical areas of the adult rat. Neuroscience 120:5-20.
12. Fukuda T, Kosaka T, Singer W, Galuske RAW (2006) Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci 26:3434-3443.
13. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH (2002) Multicolor and electron microscopic imaging of connexin trafficking. Science 296:503-507.
14. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
15. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2:425-433.
16. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
17. Graybiel AM, Chesselet MF (1984) Compartmental distribution of striatal cell bodies expressing [Met]enkephalin-like immunoreactivity. Proc Natl Acad Sci U S A 81:7980-7984.
18. Groves PM, Martone M, Young SJ, Armstrong DM (1988) Three-dimensional pattern of enkephalin-like immunoreactivity in the caudate nucleus of the cat. J Neurosci 8:892-900.
19. Harting JK, Updyke BV, Van Lieshout DP (2001) Striatal projections from the cat visual thalamus. Eur J Neurosci 14:893-896
20. Jinno S, Aika Y, Fukuda T, Kosaka T (1998) Quantitative analysis of GABAergic neurons in the mouse hippocampus, with optical disector using confocal laser scanning microscope. Brain Res 814:55-70.
21. Jordan K, Chodock R, Hand AR, Laird DW (2001) The origin of annular junctions: a mechanism of gap junction internalization. J Cell Sci 114:763-773.
22. Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 72:363-370.
23. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
24. Kita H, Kosaka T, Heizmann CW (1990) Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536:1-15.
25. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
26. Kosaka T (1983) Gap junctions between non-pyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions). Brain Res 271:157-161.
27. Kosaka T, Kosaka K (2005) Intraglomerular dendritic link connected by gap junctions and chemical synapses in the mouse main olfactory bulb: electron microscopic serial section analysis. Neuroscience 131:611-625.
28. Kubota Y, Kawaguchi Y (1993) Spatial distribution of chemically identified intrinsic neurons in relation to patch and matrix compartments of rat neostriatum. J Comp Neurol 332:499-513.
29. 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.
30. Larsen WJ, Hai-Nan (1978) Origin and fate of cytoplasmic gap junctional vesicles in rabbit granulose cells. Tissue Cell 10:585-598.
31. Makowski L, Caspar DL, Phillips WC, Goodenough DA (1977) Gap junction structures: II. Analysis of the X-ray diffraction data. J Cell Biol 74:629-645.
32. Malach R, Graybiel AM (1986) Mosaic architecture of the somatic sensory-recipient sector of the cat's striatum. J Neurosci 6:3436-3458.
33. Muller JF, Mascagni F, McDonald AJ (2005) Coupled networks of parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Neurosci 25:7366-7376.
34. Nagy A, Paróczy Z, Norita M, Benedek G (2005) Multisensory responses and receptive field properties of neurons in the substantia nigra and in the caudate nucleus. Eur J Neurosci 22:419-424.
35. Nagy A, Eördegh G, Paróczy Z, Márkus Z, Benedek G (2006) Multisensory integration in the basal ganglia. Eur J Neurosci 24:917-924.
36. Norita M, McHaffie JG, Shimizu H, Stein BE (1991) The corticostriatal and corticotectal projections of the feline lateral suprasylvian cortex demonstrated with anterograde biocytin and retrograde fluorescent techniques. Neurosci Res 10:149-155.
37. Parent A (1990) Extrinsic connections of the basal ganglia. Trends Neurosci 13:254-258.
38. Rash JE, Staines WA, Yasumura T, Patel D, Furman CS, Stelmack GL, Nagy JI (2000) Immunogold evidence that neuronal gap junctions in adult brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc Natl Acad Sci U S A 97:7573-7588.
39. Selemon LD, Goldman-Rakic PS (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5:776-794.
40. Sloper JJ, Powell TPS (1978) Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex. Proc R Soc Lond B Biol Sci 203:39-47.
41. Söhl G, Degen J, Teubner B, Willecke K (1998) The murine gap junction gene connexin36 is highly expressed in mouse retina and regulated during brain development. FEBS Letters 428:27-31.
42. Sotelo C, Korn H (1978) Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int Rev Cytol 55:67-107.
43. Sotelo C, Palay SL (1970) The fine structure of the lateral vestibular nucleus in the rat: II. Synaptic organization. Brain Res 18:93-115.
44. Sotelo C, Llinas R, Baker R (1974) Structural study of inferior olivary nucleus of the cat: morphological correlates of electron coupling. J Neurophysiol 37:541-559.
45. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using disector. J Microsc 134:127-136.
46. Tepper JM, Koós T, Wilson CJ (2004) GABAergic microcircuits in the neostriatum. Trends Neurosci 27:662-669.
47. Traub RD, Bibbig A, LeBeau FE, Buhl EH, Whittington MA (2004) Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. Annu Rev Neurosci 27:247-278.
48. Updyke BV (1993) Organization of visual corticostriatal projections in the cat, with observations on visual projections to claustrum and amygdala. J Comp Neurol 327:159-193.
49. Zsiros V, Maccaferri G (2005) Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J Neurosci 25:8686-8695.
50. Zsiros V, Aradi I, Maccaferri G (2007) Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus. J Physiol 576:527-544.