Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat

Journal of Neuroscience

Volumn 18, Issue 11, 1998, Pages 4255-4270

  Tamás, Gábor ^a,b   Somogyi, Peter ^a   Buhl, Eberhard H ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Cerebral cortex; GABA; Inhibition; Interneuron; IPSP; Synapse

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CAT; CELL INTERACTION; CELL SYNCHRONIZATION; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 0032101758     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-11-04255.1998     Document Type: Article

References (62)

1. Acsady L, Gores TJ, Freund TF (1996) Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73:317-334.
2. Ahmed B, Anderson JC, Martin KAC, Nelson JC (1997) Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J Comp Neurol 380:230-242.
3. Andersen P, Eccles JC, Loyning Y (1963) Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 198:540-542.
4. Anderson JC, Douglas RJ, Martin KAC, Nelson JC (1994) Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J Comp Neurol 341:25-38.
5. Avoli M (1986) Inhibitory potentials in neurons of the deep layers of the in vitro neocortical slice. Brain Res 370:165-170.
6. Azouz R, Gray CM, Nowak LG, McCormick DA (1997) Physiological properties of inhibitory interneurons in cat striate cortex. Cereb Cortex 7:534-545.
7. Benardo LS (1994) Separate activation of fast and slow inhibitory postsynaptic potentials in rat neocortex in vitro. J Physiol (Lond) 476:203-215.
8. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
9. Buhl EH, Cobb SR, Halasy K, Somogyi P (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7:1989-2004.
10. Buhl EH, Tamas G, Szilagyi T, Stricker C, Paulsen O, Somogyi P (1997) Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. J Physiol (Lond) 500:689-713.
11. Bush P, Sejnowski T (1996) Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic network models. J Comp Neurosci 3:91-110.
12. Buzsaki G, Chrubak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504-510.
13. Buzsaki G, Penttonen M, Nadasdy Z, Bragin A (1996) Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc Natl Acad Sci USA 93:9921-9925.
14. 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.
15. Cobb SR, Halasy K, Vida I, Nyiri G, Tamas G, Buhl EH, Somogyi P (1997) Synaptic effects of identified interneurones innervating both interneurones and pyramidal cells in the rat hippocampus. Neuroscience 79:629-648.
16. Connors BW, Malenka RC, Suva LR (1988) Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. J Physiol (Lond) 406:443-468.
17. Deuchars J, Thomson AM (1995) Single axon fast inhibitory postsynaptic potentials elicited by a sparsely spiny interneuron in rat neocortex. Neuroscience 65:935-942.
18. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
19. Freund TF, Meskcnaite V (1992) γ-Aminobutyric acid-containing basal forebrain neurons innervate inhibitory interneurons in the neocortex. Proc Natl Acad Sci USA 89:738-742.
20. Freund TF, Martin KAC, Smith AD, Somogyi P (1983) Glutamate decarboxylase-immunoreactive terminals of Golgi-impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex. J Comp Neurol 221:263-278.
21. Freund TF, Magloczky Zs, Soltesz I, Somogyi P (1986) Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat. Neuroscience 19:1133-1159.
22. Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280:120-125.
23. Ginsborg BL (1973) Electrical changes in the membrane in junctional transmission. Biochim Biophys Acta 300:289-317.
24. Gray EG (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420-433.
25. Gulyas AI, Miles R, Hajos N, Freund TF (1993) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5:1729-1751.
26. Gulyas AI, Hajos N, Freund TF (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
27. Halasy K, Somogyi P (1993) Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:411-429.
28. Han Z-S, Buhl EH, Lorinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyms of the rat hippocampus. Eur J Neurosci 5:395-410.
29. Jagadeesh B, Gray CM, Ferster D (1992) Visually evoked oscillations of membrane potential in cells of cat visual cortex. Science 257:552-554.
30. Jefferys JGR, Traub RD, Whittington MA (1996) Neuronal networks for induced "40 Hz" rhythms. Trends Neurosci 19:202-208.
31. Kisvarday ZF, Martin KAC, Whitteridge D, Somogyi P (1985) Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol 241:111-137.
32. Kisvarday ZF, Beaulieu C, Eysel UT (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition. J Comp Neurol 327:398-415.
33. Kisvarday ZF, Kim D-S, Eysel UT, Bonhoeffer T (1994) Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex. Eur J Neurosci 6:1619-1632.
34. Korn H, Mallet A, Triller A, Faber DS (1982) Transmission at a central inhibitory synapse. II. Quantal description of release, with a physical correlate for binomial n. J Neurophysiol 48:679-707.
35. Lytton WW, Sejnowski TJ (1991) Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol 66:1059-1079.
36. Martin KAC, Somogyi P, Whitteridge D (1983) Physiological and morphological properties of identified basket cells in the cat's visual cortex. Exp Brain Res 50:193-200.
37. Mason A, Nicoll A, Stratford K (1991) Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J Neurosci 11:72-84.
38. McCormick DA, Connors BW, Lightall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
39. Meskenaite V (1997) Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 379:113-132.
40. Miles R, Wong RKS (1987) Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol (Lond) 388:611-629.
41. Miles R, Toth K, Gulyas AI, Hajos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
42. Nunzi MG, Gorio A, Milan F, Freund TF, Somogyi P, Smith AD (1985) Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and non-pyramidal neurons in the hippocampus. J Comp Neurol 237:485-505.
43. Ramon y Cajal S (1894) La fine structure des centres nerveux. Proc R Soc Lond [Biol] 55:444-468.
44. Sik A, Penttonen M, Ylinen A, Buzsaki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651-6665.
45. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555-586.
46. A receptors in the lateral geniculate nucleus and visual cortex. In: Proc Retina Res Found Symp, Vol 2, Neural mechanisms of visual perception (Lam DK-T, Gilbert CD, eds), pp 35-62. The Woodlands, TX: Portfolio.
47. Somogyi P, Cowey A (1981) Combined Golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. J Comp Neurol 195:547-566.
48. Somogyi P, Soltesz I (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket celts and clutch cells in the cat's visual cortex. Neuroscience 19:1051-1065.
49. Somogyi P, Kisvarday ZF, Martin KAC, Whitteridge D (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261-294.
50. Szentagothai J, Arbib MA (1974) Conceptual models of neural organization. Neurosci Res Prog Bull 12:305-510.
51. Tamas G, Buhl EH, Somogyi P (1995) Synaptic responses and effect of physiologically and anatomically identified double bouquet cells in cat visual cortex. Eur J Neurosci [Suppl] 8:76.
52. Tamas G, Buhl EH, Jones RSG, Somogyi P (1997a) Interactions between distinct GABAergic neuron types eliciting fast IPSPs in cat visual cortex: number and placement of synapses. Soc Neurosci Abstr 23:1265.
53. Tamas G, Buhl EH, Somogyi P (1997b) Fast IPSPs elicited via multiple synaptic release sites by distinct types of GABAergic neurone in the cat visual cortex. J Physiol (Lond) 500:715-738.
54. Tamas G, Buhl EH, Somogyi P (1997c) Massive autaptic self-innervation of GABAergic neurons in cat visual cortex. J Neurosci 17:6352-6364.
55. Thomson AM, West DC, Hahn J, Deuchars J (1996) Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol (Lond) 496:81-102.
56. Traub RD, Jefferys JGR, Miles R, Whittington MA, Toth K (1994) A branching dendritic model of a rodent CA3 pyramidal neurone. J Physiol (Lond) 481:79-95.
57. TraubRD, Whittington MA, Stanford IM, Jefferys JGR (1996) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621-624.
58. i changes in the dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 76:2896-2906..
59. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at the stratum-radiatum lacunosum-moleculare border in the CA1 area of the hippocampus in vitro. J Physiol (Lond) 506:755-773.
60. Wang X-J, Buzsaki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16:6402-6413.
61. Whittington MA, Traub RD, Jefferys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
62. Ylinen A, Soltesz I, Bragin A, Penttonen M, Sik A, Buzsaki G (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.