Innervation of VIP-immunoreactive neurons by the ventroposteromedial thalamic nucleus in the barrel cortex of the rat

Journal of Comparative Neurology

Volumn 367, Issue 2, 1996, Pages 194-204

  Staiger, Jochen F ^a,b   Zilles, Karl ^b   Freund, Tamás F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

asymmetric synapses; interneurons; laminar organization; somatosensory cortex; thalamocortical connections

Indexed keywords

4 AMINOBUTYRIC ACID; LEUKOAGGLUTININ; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; ELECTRON MICROSCOPY; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; T LYMPHOCYTE SUBPOPULATION; THALAMUS NUCLEUS;

AFFERENT PATHWAYS; ANIMALS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; NEURONS; PHYTOHEMAGGLUTININS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; THALAMIC NUCLEI; VASOACTIVE INTESTINAL PEPTIDE;

EID: 0029984517     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960401)367:2<194::AID-CNE3>3.0.CO;2-0     Document Type: Article

References (59)

1. Agmon, A., and B.W. Connors (1992) Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J. Neurosci. 12:319-329.
2. Armstrong-James, M., C A. Callahan, and M.A Friedman (1991) Thalamocortical processing of vibrissal information in the rat. I. Intracortical origins of surround but not centre-receptive fields of layer IV neurones in the rat S1 barrel field cortex. J. Comp. Neurol. 303:193-210.
3. Benshalom, G., and E L. White (1986) Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex. J Comp. Neurol. 253:303-314.
4. Besson, J , A Sarrieau, M. Vial, J.-C. Marie, G Rosselin, and W. Rostene (1986) Characterization and autoradiographic distribution of vasoactive intestinal peptide binding sites in the rat central nervous system Brain Res. 398:329-336.
5. Chedotal, A., C. Cozzari, M.-P Faure, B.K. Hartman, and E. Hamel (1994a) Distinct choline acetltransferase (ChAT) and vasoactive intestinal polypeptide bipolar neurons project to local blood vessels in the rat cerebral cortex. Brain Res. 646:181-193.
6. Chedotal. A., D. Umbriaco, L. Descarries, B.K. Hartman, and E. Hamel (1994b) Light and electron microscopic immunocytochemical analysis of the neurovascular relationships of choline acetyltransferase and vasoactive intestinal polypeptide nerve terminals in the rat cerebral cortex. J. Comp. Neurol. 543:57-71.
7. Csillag, A., F. Hajós, K. Zilles, A. Schleicher, and H. Schroeder (1993) Matching localization of vasoactive intestinal polypeptide (VIP) and VIP-receptor at presynaptic and postsynaptic sites in the mouse visual cortex. J. Neurocytol. 22:491-497.
8. DeFelipe, J. (1993) Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters. neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb. Cortex 3:271-289.
9. Di, S., C Baumgartner, and D.S. Barth (1990) Laminar analysis of extracellular field potentials in rat vibrissa/barrel cortex. J. Neurophysiol. 63:832-840.
10. Dykes, R.W., P. Landry, R Metherate, and T.P Hicks (1984) Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J. Neurophysiol. 52:1066-1093.
11. Eckenstein, F , and R.W. Baughman (1984) Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide. Nature 309:153-155.
12. Fahrenkrug, J., and O.B. Schaflalitzky de Muckadell (1978) Distribution of vasoactive intestinal polypeptide (VIP) in the porcine central nervous system. J. Neurochem. 31:1445-1451
13. Ferron, A., G.R. Siggins, and F.E. Bloom (1985) Vasoactive intestinal polypeptide acts synergistically with norepinephrine to depress spontaneous discharge rate in cerebral cortical neurons Proc. Natl. Acad. Sci. USA 82:8810-8812.
14. Gerfen, C.G., and P E. Sawchenko (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 290:219-238.
15. Giachetti, A., S.I. Said, R C. Reynolds, and F.C. Koniges (1977) Vasoactive intestinal polypeptide in brain: localization in and release from isolated nerve terminals Proc. Natl. Acad. Sci. USA 74:3424-3428.
16. Glassman, R.B. (1994) Behavioral specializations of SI and SII cortex: a comparative examination of the neural logic of touch in rats, cats, and other mammals. Exptl. Neurol. 125:134-141.
17. Groenewegen, H.J , and F.G. Wouterlood (1990) Light and electron microscopic tracing of neuronal connections with Phaseolus vulgaris-leucoagglutinin (PHA-L), and combinations with other neuroanatomical techniques. In A. Björklund, T. Hokfelt, F.G Wouterlood, and A. van den Pol (eds): Handbook of Chemical Neuroanatomy, Vol 8: Analysis of Neuronal Synaptic Interactions and Microcircuits. Amsterdam: Elsevier Science Publishers B V , pp 47-124.
18. Gulyás, A.I., T.J. Görcs, and T.F. Freund (1990) Innervation of different peptide-containing neurons in the hippocampus by GABAergic septal afferents. Neuroscience 37.31-44
19. Gulyás , A.I., R. Miles, A. Sik, K Toth, N. Tamamaki, and T.F. Freund (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366: 683-687
20. Hajós, F., K. Zilles, A. Schleicher, and M. Káimán (1988) Types and spatial distribution of vasoactive intestinal polypeptide (VIP)-containing synapses in the rat visual cortex. Anat. Embryol 178 207-217.
21. Harris, R.M., and T.A. Woolsey (1983) Computer-assisted analyses of barrel neuron axons and their putative synaptic contacts. J. Comp. Neurol 220:63-79.
22. Hersh, S.M , and EL White (1981) Thalamoeortical synapses involving identified neurons in mouse primary somatosensory cortex: a terminal degeneration and Golgi/EM study. J. Comp. Neurol. 195:253-263.
23. Jensen, K.F., and H.P. Killackey (1987) Terminal arbors of axons projecting to the somatosensory cortex of the adult rat I. The normal morphology of specific thalamocortical afferents. J. Neurosci. 7.3529-3543.
24. Kawaguchi, Y., and Y. Kubota (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindin D28k-unmunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70:387-396
25. Keller, A., E.L White, and P.E. Cipolloni (1985) The identification of thalamocortical axon terminals in barrels of mouse SmI cortex using immunohistoehemistry of anterogradely transported lectin (Phaseolus vulgaris-leueoagglutinin). Brain Res. 343:159-165.
26. Killackey, H P. (1973) Anatomical evidence for cortical subdivisions based on vertically discrete thalamic projections from the ventral posterior nucleus to cortical barrels in the rat. Brain Res. 51:326-331.
27. Kubota, Y., R Hattori, and Y. Yui (1994) Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res. 649:159-173.
28. Kyriazi, H.T., G.E. Carvell, Q. Zhou, and D.J. Simons (1993) Bicuculline-induced receptive field changes in real and simulated barrel neurons. Soc. Neurosci. 19:49.11.
29. Loren, I., P.C Emson, J. Fahrenkrug, A. Björklund, J Alumets, R. Hakanson, and F Sundler (1979) Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience 4:1953-1976.
30. Lu, S., and R.C. Lin (1993) Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens. Motor Res. 10:1-16.
31. Ma, P.M (1991) The barrelettes - architectonic vibrissal representations in the brainstem trigeminal complex of the mouse. I. Normal structural organization. J. Comp. Neurol. 309:161-199.
32. Magistretti, P.J., J.H. Morrison, W.J. Shoemaker, and F.E. Bloom (1981) Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc. Natl. Acad. Sci. USA 78:6535-6539.
33. Martin, J.-L., M.M. Dietl, P.R. Hof, J.M. Palacios, and P.J. Magistretti (1987) Autoradiographic mapping of [mono[125I]iodo-tyr10, met[O17]vasoaetive intestinal peptide binding sites in the rat brain. Neuroscience 23:539-565.
34. McCasland, J.S., and T.A. Woolsey (1988) High-resolution 2-deoxyglucose mapping of functional cortical columns in mouse barrel cortex. J. Comp. Neurol. 278:555-569.
35. McCormick, D.A., Z. Wang, and J. Huguenard (1993) Neurotransmitter control of neocortical neuronal activity and excitability. Cereb. Cortex 3:387-398.
36. Morrison. J.H. P J. Magistretti, R. Benoit, and F.E. Bloom (1984) The distribution and morphological characteristics of the intracortical VIP-positive cell: an immunohistochemical analysis. Brain Res. 292:269-282.
37. Mountcastle, V.B. (1979) An organizing principle for cerebral function: the unit module and the distributed system. In F.O. Schmitt and F.G. Worden (eds). The Neurosciences Fourth Study Program. Cambridge, MA: MIT Press, pp. 21-42.
38. Murphy, P.C., K.L. Grieve, and A.M. Silito (1993) Effects of vasoactive intestinal polypeptide on the response properties of cells in area 17 of the cat visual cortex. J. Neurophysiol. 69:1465-1474.
39. Oh, J D., N.J. Woolf, A. Roghani, R.H. Edwards, and L.L. Butcher (1992) Chohnergic neurons in the rat central nervous system demonstrated by in situ hybridization of choline acetyltransferase mRNA. Neuroscience 47:807-822
40. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates, 2nd ed. Sydney Academic Press.
41. Peters, A. (1990) The axons terminais of vasoactive intestinal polypeptide (VIP)-containing bipolar cells in rat visual cortex. J. Neurocytol. 19:672-685.
42. Peters, A., and K.M. Harriman (1988) Enigmatic bipolar cell of rat visual cortex. J. Comp. Neurol. 267 409-432.
43. Phillis, J.W, J.R Kirkpatrick, and S.I. Said (1978) Vasoactive intestinal polypeptide excitation of central neurons Can. J. Physiol Pharmacol. 56:337-340.
44. Quik, M , L.L. Iversen, and S.R Bloom (1978) Effect of vasoactive intestinal peptide (VIP) and other peptides on cAMP accumulation in rat brain. Biochem. Pharmacol. 27.2209-2213.
45. Sessler, F M., S.M. Grady, B.D. Waterhouse, and H.C Moises (1991) Electrophysiological actions of VIP in rat somatosensory cortex. Peptides 12:715-721.
46. Simons, D.J. (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol. 41.798-820.
47. Simons, D.J., and G.E. Carvell (1989) Thalamocortical response transformation m the rat vibrissa/barrel system. J Neurophysiol. 61:311-330.
48. Szentágothai J. (1975) The module-concept in cerebral cortex architecture. Brain Res. 95:475-496.
49. van der Loos, H. (1976) Barreloids in mouse somatosensory thalamus. Neurosci. Lett. 2:1-6
50. Wang, J.-Y., T.L. Yaksh, and V.L.W. Go (1985) Studies on the in vivo release of vasoactive intestinal polypeptide (VIP) from the cerebral cortex: effects of cortical, brainstem and somatic stimuli Brain Res 326 317-334.
51. Welker, C. (1971) Microelectrode delineation of fine grain somatotupic organization of SmI cerebral neocortex in albino rat Brain Res 26 259-275.
52. Welker, C., and T.A Woolsey (1974) Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse J Comp. Neurol. 158 437-454
53. White, E.L. (1978) Identified neurons in mouse SmI cortex which are postsynaptic to thalamocortical axon terminals a combined Golgielectron microscopic and degeneration study J Comp Neurol 181.627-662
54. White, E.L. (1986) Terminations of thalamic afferents in the cerebral cortex In E.G Jones and A Peters (eds) Cerebral Cortex. Vol 5 Sensory-Motor Areas and Aspects of Cortical Connectivitv New York Plenum Press, pp 271-289
55. White, E L , and S.M. Hersh (1982) A quantitative study of thalamocortical and other synapses involving the apical dendrites of corticothalamic projection cells in mouse SmI cortex J. Neurocytol. 11:137-157
56. White E L , and M P Rock (1981) A comparison of thalamocortical and other synaptic inputs to dendrites of two non-spiny neurons in a single barrel of mouse SmI cortex. J. Comp. Neurol. 195:265-277.
57. Williams, M X , D S Zahm, and M.F. Jacquin (1994) Differential foci and synaptic organization of the principal and spinal trigeminal projections to the thalamus in the rat. Eur J. Neurosci. 6:429-453.
58. Woolsey, T A , and H. van der Loos (1970) The structural organization of laver IV in the somatosensory region (SI) of mouse cerebral cortex Brain Res 17:205-242
59. Zilles K , F Hajós, A. Csillag, M. Kálmán, P. Sótonyi, and A. Schleicher (1993) Vasoactive intestinal polypeptide immunoreactive structures in the mouse barrel field Brain Res. 618:149-154.