Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex

Journal of Neuroscience

Volumn 25, Issue 27, 2005, Pages 6278-6285

  Simon, Anna ^a   Oláh, Szabolcs ^a   Molnár, Gábor ^a   Szabadics, János ^a   Tamás, Gábor ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Basket cell; Cerebral cortex; GABAB receptor; GABAergic neuron; Gap junction; Interneuron

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL TYPE; GAP JUNCTION; GLIA CELL; HISTOLOGY; INTERNEURON; NEOCORTEX; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; SYNAPSE;

ACTION POTENTIALS; ANIMALS; CELL COMMUNICATION; EVOKED POTENTIALS; GAP JUNCTIONS; INTERNEURONS; NEOCORTEX; NEUROGLIA; PYRAMIDAL CELLS; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GABA-B; SOMATOSENSORY CORTEX;

EID: 21844440009     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1431-05.2005     Document Type: Article

References (51)

1. 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.
2. Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495-511.
3. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H (2003) A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38:805-817.
4. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G (2003) Selective impairment of hippocampal γ oscillations in connexin-36 knock-out mouse in vivo. J Neurosci 23:1013-1018.
5. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical non-pyramidal cells. J Neurosci 17:3894-3906.
6. Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E (2000) Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci USA 97:6144-6149.
7. Chow CC, Kopell N (2000) Dynamics of spiking neurons with electrical coupling. Neural Comput 12:1643-1678.
8. Chu Z, Galarreta M, Hestrin S (2003) Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23:96-102.
9. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
10. Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393-418.
11. Connors BW, Benardo LS, Prince DA (1984) Carbon dioxide sensitivity of dye coupling among glia and neurons of the neocortex. J Neurosci 4:1324-1330.
12. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31:477-485.
13. Demb JB, Pugh EN (2002) Connexin36 forms synapses essential for night vision. Neuron 36:551-553.
14. 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.
15. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
16. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2:425-433.
17. Gibson JF, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
18. Guldenagel M, Ammermuller J, Feigenspan A, Teubner B, Degen J, Sohl G, Willecke K, Weiler R (2001) Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36. J Neurosci 21:6036-6044.
19. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
20. Gutnick MJ, Prince DA (1981) Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. Science 211:67-70.
21. Hestrin S, Armstrong WE (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16:5290-5300.
22. Hornstein EP, Verweij J, Schnapf JL (2004) Electrical coupling between red and green cones in primate retina. Nat Neurosci 7:745-750.
23. Jones EG (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J Comp Neurol 160:205-268.
24. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
25. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
26. Kim U, Sanchez-Vives MV, McCormick DA (1997) Functional dynamics of GABAergic inhibition in the thalamus. Science 278:130-134.
27. Kisvarday ZF, Gulyas A, Beroukas D, North JB, Chubb IW, Somogyi P (1990) Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain 113:793-812.
28. Knowles WD, Funch PG, Schwartzkroin PA (1982) Electrotonic and dye coupling in hippocampal CA1 pyramidal cells in vitro. Neuroscience 7:1713-1722.
29. Kopell N, Ermentrout B (2004) Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proc Natl Acad Sci USA 101:15482-15487.
30. Lee EJ, Han JW, Kim HJ, Kim IB, Lee MY, Oh SJ, Chung JW, Chun MH (2003) The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur J Neurosci 18:2925-2934.
31. Long MA, Deans MR, Paul DL, Connors BW (2002) Rhythmicity without synchrony in the electrically uncoupled inferior olive. J Neurosci 22:10898-10905.
32. Mody I, De Koninck Y, Otis TS, Soltesz I (1994) Bridging the cleft at GABA synapses in the brain. Trends Neurosci 17:517-525.
33. Ramon y Cajal S (1904) Textura del systema nervioso del nombre y los vertebrados. Madrid: Imprenta y Librería de Nicolás Moya.
34. Roerig B, Feller MB (2000) Neurotransmitters and gap junctions in developing neural circuits. Brain Res Brain Res Rev 32:86-114.
35. Sancesario G, Pisani A, D'Angelo V, Calabresi P, Bernardi G (1998) Morphological and functional study of dwarf neurons in the rat striatum. Eur J Neurosci 10:3575-3583.
36. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31:831-840.
37. Sherman A, Rinzel J (1992) Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc Natl Acad Sci USA 89:2471-2474.
38. Sloper JJ (1972) Gap junctions between dendrites in the primate neocortex. Brain Res 44:641-646.
39. Sohl G, Maxeiner S, Willecke K (2005) Expression and functions of neuronal gap junctions. Nat Rev Neurosci 6:191-200.
40. Somogyi P (1977) A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res 136:345-350.
41. Somogyi P (1989) Synaptic organisation of GABAergic neurons and GABAA receptors in the lateral geniculate nucleus and visual cortex. In: Neural mechanisms of visual perception (Lam DK-T, Gilbert CD, eds), pp 35-62. Houston: Portfolio.
42. Szabadics J, Lorincz A, Tamas G (2001) β and γ frequency synchronizationby dendritic GABAergic synapses and gap junctions in a network of cortical interneurons. J Neurosci 21:5824-5831.
43. Szentagothai J, Arbib MA (1974) Conceptual models of neural organization. Neurosci Res Prog Bull 12:305-510.
44. Tamas G, Buhl EH, Somogyi P (1997) Fast IPSPs elicited via multiple synaptic release sites by distinct types of GABAergic neuron in the cat visual cortex. J Physiol (Lond) 500:715-738.
45. Tamas G, Buhl EH, Lorincz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3:366-371.
46. Tamas G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902-1905.
47. Tamas G, Szabadics J, Lorincz A, Somogyi P (2004) Input and frequency-specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin. Eur J Neurosci 20:2681-2690.
48. Thomson AM, Destexhe A (1999) Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices. Neuroscience 92:1193-1215.
49. Traub RD, Pais I, Bibbig A, LeBeau FE, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA (2003) Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc Natl Acad Sci USA 100:1370-1374.
50. Valverde F (1971) Short axon neuronal subsystems in the visual cortex of the monkey. Int J Neurosci 1:181-197.
51. Venance L, Rozov A, Blatow M, Burnashev N, Feldmeyer D, Monyer H (2000) Connexin expression in electrically coupled postnatal rat brain neurons. Proc Natl Acad Sci USA 97:10260-10265.