Glutamate decarboxylase immunoreactivity in corticocortical projecting neurons of rat somatic sensory cortex

Neuroscience

Volumn 72, Issue 2, 1996, Pages 435-448

  Fabri, M ^a   Manzoni, T ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

immunocytochemistry; inhibitory connections; retrograde tracing; rodents; somatosensory areas

Indexed keywords

GLUTAMATE DECARBOXYLASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GABAERGIC SYSTEM; IMMUNOCYTOCHEMISTRY; MALE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX;

EID: 0029987026     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(95)00568-4     Document Type: Article

References (80)

1. Akers R. M. and Killackey H. P. (1978) Organization of corticocortical connections in the parietal cortex of the rat. J. comp. Neurol. 181, 513-538.
2. Akhtar N. D. and Land P. W. (1988) Laminar distribution of glutamate decarboxylase immunoreactivity in the rat SmI cortex. Soc. Neurosci. Abstr. 14, 717.
3. Akhtar N. D. and Land P. W. (1991) Activity-dependent regulation of glutamic acid decarboxyase in the rat barrel cortex: effect of neonatal versus adult sensory deprivation. J. comp. Neurol. 307, 200-213.
4. Albus K. and Wahle P. (1994) The topography of tangential inhibitory connections in the postnatally developing and mature striate cortex of the cat. Eur. J. Neurosci. 6, 779-792.
5. Albus K., Wahle P., Lübke J. and Matute C. (1991) The contribution of GABA-ergic neurons to horizontal intrinsic connections in upper layers of the cat's striate cortex. Brain Res. 85, 235-239.
6. Alloway K. D., Rosenthal P. and Burton H. (1989) Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats. Expl Brain Res. 78, 514-532.
7. Asanuma H., Waters R. S. and Yumiya H. (1982) Physiological properties of neurons projecting from area 3a to area 4γ of feline cerebral cortex. J. Neurophysiol. 48, 1048-1057.
8. Basbaum A. I. and Ménétrey D. (1987) Wheat germ agglutinin-apo HRP gold: a new retrograde tracer for light- and electron-microscopic single- and double-label studies. J. comp. Neurol. 261, 306-318.
9. Beaulieu C. (1993) Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res. 609, 284-292.
10. Beaulieu C., Campistron G. and Crevier C. (1994) Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat. J. comp. Neurol. 339, 559-572.
11. Burton H. (1986) Second somatosensory cortex and related areas. In Cerebral Cortex (eds Peters A. and Jones E. G.), Vol. 5, Sensory-motor Areas and Aspect of Cortical Connectivity, pp. 31-98. Plenum, New York.
12. Burton H. and Robinson C. J. (1987) Responses in the first or second somatosensory cortical area in cats during transient inactivation of the other ipsilateral area with lidocaine hydrochloride. Somatosensory Res. 4, 215-236.
13. Burton H., Sathian K. and Shao Dian-Hua (1990) Altered responses to cutaneous stimuli in the second somatosensory cortex following lesions of the postcentral gyrus in infant and juvenile macaques. J. comp. Neurol. 291, 395-414.
14. Chang Y.-C. and Gottlieb D. I. (1988) Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J. Neurosci. 8, 2123-2130.
15. Chapin J. K. and Lin C.-S. (1984) Mapping the body representation in SI cortex of anesthetized and awake rats. J. comp. Neurol. 229, 199-213.
16. Chapin J. K. and Lin C.-S. (1990) The somatic sensory cortex of rat. In The Cerebral Cortex of the Rat (eds Kolb B. and Tees R. C.), pp. 341-380. MIT Press, Cambridge, MA.
17. Chapin J. K., Sadeq M. and Guise J. L. U. (1987) Corticocortical connections within the primary somatosensory cortex of the rat. J. comp. Neurol. 263, 326-346.
18. Chmielowska J., Stewart M. G., Bourne R. C. and Hamori J. (1986) γ-Aminobutyric acid immunoreactivity in mouse barrel field: a light microscopical study. Brain Res. 368, 371-374.
19. Chmielowska J., Stewart M. G. and Bourne R. C. (1988) γ-Aminobutyric acid (GABA) immunoreactivity in mouse and rat first somatosensory (SI) cortex: description and comparison. Brain Res. 439, 155-168.
20. Chudler E. H., Pretel S. and Kenshalo D. R. Jr (1988) Distribution of GAD-immunoreactive neurons in the first (SI) and second (SII) somatic sensory cortex of monkey. Brain Res. 456, 57-63.
21. Cobas A., Welker E., Fairén A., Kraftsik R. and Van Der Loos H. (1987) GABAergic neurons in the barrel cortex of the mouse: an analysis using neuronal archetypes. J. Neurocytol. 16, 843-871.
22. Colonnier M. (1981) The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In The Organization of the Cerebral Cortex (eds Schmidt F. O., Worden F. G. and Dennis S. G.), pp. 125-152. MIT Press, Cambridge, MA.
23. Conti F., Fabri M. and Manzoni T. (1988a) Glutamate-positive corticocortical neurons in the somatic sensory areas I and II of cats. J. Neurosci. 8, 2948-2960.
24. Conti F., Fabri M. and Manzoni T. (1988b) Immunocytochemical evidence for glutamatergic cortico-cortical connections in monkeys. Brain Res. 462, 148-153.
25. Conti F., Fabri M. and Manzoni T. (1988c) Aspartate-positive cortico-cortical neurons in the somatic sensory areas 1 and II of cats. In Frontiers in Excitatory Amino Acids (eds Cavalheiro E. A., Lehmann J. and Turski L.), pp. 133-136. Alan R. Liss, New York.
26. DeFelipe J. and Fariñas I. (1992) The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39, 563-607.
27. DeFelipe J. and Jones E. G. (1985) Vertical organization of γ-aminobutyric acid-accumulating intrinsic neuronal system in monkey cerebral cortex. J. Neurosci. 5, 3246-3260.
28. Doetsch G. S., Norelle A., Mark E. K., Standage G. P., Lu S. M. and Lin R. C. S. (1993) Immunoreactivity for GAD and three peptides in somatosensory cortex and thalamus of racoon. Brain Res. Bull. 31, 553-563.
29. Dykes R. W., Landry P., Metherate R. and Hicks T. P. (1984) Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J. Neurophysiol. 52, 1066-1093.
30. Elhanany E. and White E. L. (1990) Intrinsic circuits: synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J. comp. Neurol. 291, 43-54.
31. Esclapez M., Campistron G. and Trottier S. (1987) Immunocytochemical localization and morphology of GABA-containing neurons in the prefrontal and frontoparietal cortex of the rat. Neurosci. Lett. 77, 131-136.
32. Esclapez M., Tillakaratne N. J. K., Kaufman D. L., Tobin A. J. and Houser C. R. (1994) Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the two forms. J. Neurosci. 14, 1834-1855.
33. Fabri M. and Burton H. (1991a) Topography of connections between primary somatosensory cortex and posterior complex in rat: a multiple fluorescent tracer study. Brain Res. 538, 351-357.
34. Fabri M. and Burton H. (1991b) Ipsilateral cortical connections of primary somatic sensory cortex in rats. J. comp. Neurol. 311, 405-424.
35. Fabri M., Natalini F. and Manzoni T. (1995) GAD-positive neurons in the associative projections from the second to the first somatic sensory cortex in rats. Pflügers Arch. 430, R204.
36. Fairén A., Cobas A. and Fonseca M. (1986) Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J. comp. Neurol. 251, 67-83.
37. Fisher R. S., Buchwald N. A., Hull C. D. and Levine M. S. (1986) The GABAergic striatonigral neurons of the cat: demonstration by double peroxidase labeling. Brain Res. 398, 148-156.
38. Fisher R. S., Buchwald N. A., Hull C. D. and Levine M. S. (1988) GABAergic basal forebrain neurons project to the neocortex: the localization of glutamic acid decarboxylase and choline acetyltransferase in feline corticopetal neurons. J. camp. Neurol. 272, 489-502.
39. Fitzpatrick D., Lund J. S., Schmechel D. E. and Towles A. C. (1987) Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. J. comp. Neurol. 264, 73-91.
40. Garraghty P. E., Pons T. P. and Kaas J. H. (1990) Ablations of areas 3b (SI proper) and 3a of somatosensory cortex in marmosets deactivate the second parietal and ventral somatic sensory areas. Somatosens. and Motor Res. 1, 125-135.
41. Ghosh S. and Porter R. (1988) Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. J. Physiol. 400, 617-629.
42. Giuffrida R. and Rustioni A. (1989) Glutamate and aspartate immunoreactivity in corticocortical neurons of the sensorimotor cortex of rats. Expl Brain Res. 74, 41-46.
43. Herman D., Kang R., MacGillis M. and Zarzecki P. (1985) Responses of cat motor cortex neurons to corticocortical and somatosensory inputs. Expl Brain Res. 57, 598-604.
44. Hicks T. P. and Dykes R. W. (1983) Receptive field size for certain neurons in primary somatosensory cortex is determined by GABA-mediated intracortical inhibition. Brain Res. 274, 160-164.
45. Houser C. R., Vaughn J. E., Hendry S. H. C., Jones E. G. and Peters A. (1984) GABA neurons in the cerebral cortex. In Cerebral Cortex (eds Peters A. and Jones E. G.), Vol. 2, Functional Properties of Cortical Cells, pp. 63-89. Plenum, New York.
46. Jones E. G. and Powell T. P. S. (1970) An electron microscopic study of the laminar pattern and mode of termination of afferent fibre pathways in the somatic sensory cortex of the cat. Phil. Trans. R. Soc. 257, 45-62.
47. Kaneko T., Caria M. A. and Asanuma H. (1994) Information processing within the motor cortex. I. Responses of morphologically identified motor cortical cells to stimulation of the somatosensory cortex. J. comp. Neurol. 345, 161-171.
48. Kaufman D. L., Houser C. R. and Tobin A. J. (1991) Two forms of the γ-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distribution and cofactor interactions. J. Neurochem. 56, 720-723.
49. Keller A. and White E. L. (1986) Distribution of glutamic acid decarboxylase-immunoreactive structures in the barrel region of mouse somatosensory cortex. Neurosci. Lett. 66, 245-250.
50. Keller A. and White E. L. (1987) Synaptic organization of GABAergic neurons in the mouse SmI cortex. J. comp. Neurol. 262, 1-12.
51. Koralek A. K., Olavarria J. and Killackey H. P. (1990) Areal and laminar organization of corticocortical projections in the rat somatosensory cortex. J. comp. Neurol. 299, 133-150.
52. Li J. and Schwark H. D. (1994) Distribution and properties of GABA-immunoreactive neurons in cat primary somatosensory cortex. J. comp. Neurol. 343, 353-361.
53. Lin C.-S., Lu S. M. and Schmechel D. E. (1985) Glutamic acid decarboxylase immunoreactivity in layer IV of barrel cortex of rat and mouse. J. Neurosci. 5, 1934-1939.
54. Lin C.-S., Lu S. M. and Schmechel D. E. (1986) Glutamic acid decarboxylase and somatostatin immunoreactivities in rat visual cortex. J. comp. Neurol. 244, 369-383.
55. Lin C.-S., Nicolelis M. A. L., Schneider J. S. and Chapin J. K. (1990) A major direct GABAergic pathway from zona incerta to neocortex. Science 248, 1553-1556.
56. Loewenstein P. R. and Somogyi P. (1991) Synaptic organization of cortico-cortical connections from the primary visual cortex to the posteromedial lateral suprasylvian visual area in the cat. J. comp. Neurol. 310, 253-266.
57. Lyon S. and Connors B. W. (1985) Distribution and forms of GABAergic neurons in rat barrel cortex: a comparative immuno- and histochemical study of GAD, GABA and GABA-transaminase. Soc. Neurosci. Abstr. 11, 751.
58. Manzoni T., Caminiti R., Spidalieri G. and Morelli E. (1979) Anatomical and functional aspects of the associative projections from somatic area SI and SII. Expl Brain Res. 34, 453-470.
59. Matsubara J. A. and Boyd J. D. (1988) Presence of GABA-immunoreactive neurons within intracortical patches in area 18 of the cat. Brain Res. 583, 161-170.
60. McDonald C. T. and Burkhalter A. (1993) Organization of long-range inhibitory connections within rat visual cortex. J. Neurosci. 13, 768-781.
61. McGuire B. A., Gilbert C. D., Rivlin P. K. and Wiesel T. N. (1991) Targets of horizontal connections in macaque primary visual cortex. J. comp. Neurol. 305, 370-392.
62. Mugnaini E. and Oertel W. H. (1985) An atlas of the distribution of GABA ergic neurons and terminals in the rat CNS as revealed by GAD immunocytochemistry. In Handbook of Chemical Neuroanatomy (eds Björklund A. and Hökfelt T.), Vol. 4, GABA and Neuropeptides in the CNS, Part 1, pp. 436-608. Elsevier, Amsterdam.
63. Murray G. M., Zhang H. Q., Kaye A. N., Sinnadurai T., Campbell D. H. and Rowe M. J. (1992) Parallel processing in rabbit first (SI) and second (SII) somatosensory cortical areas: effects of reversible inactivation by cooling of SI on responses in SII. J. Neurophysiol. 68, 703-710.
64. Oertel W. H., Schmechel D. E., Tappaz M. L. and Kopin I. J. (1981) Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6, 2689-2700.
65. Peters A. and Jones E. G. (1984) Classification of cortical neurons. In Cerebral Cortex (eds Peters A. and Jones E. G.), Vol. 1, Cellular Components of the Cerebral Cortex, pp. 107-121. Plenum, New York.
66. Pons T. P., Garraghty P. E., Friedman D. P. and Mishkin M. (1987) Physiological evidence for serial processing in somatosensory cortex. Science 237, 417-420.
67. Pons T. P., Garraghty P. E. and Mishkin M. (1992) Serial and parallel processing of tactual information in somatosensory cortex of rhesus monkeys. J. Neurophysiol. 68, 518-527.
68. Porter L. L. and Izraeli R. (1993) The effects of localized inactivation of somatosensory cortex, area 3a, on area 2 in cats. Somatosens and Motor Res. 10, 399-413.
69. Prieto J. J., Peterson B. A. and Winer J. A. (1994a) Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). J. comp. Neurol. 344, 349-382.
70. Simons D. J. (1985) Temporal and spatial integration in the rat SI vibrissa cortex. J. Neurophysiol. 54, 615-635.
71. Sloper J. J. and Powell T. P. S. (1979) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Phil. Trans. R. Soc. 285, 199-226.
72. 3H]GABA in visual cortex of rhesus monkey. Nature 294, 761-763.
73. 3H]butyric acid reveals specific interlaminar connections in the striate cortex of monkey. Proc. Natn. Acad. Sci. U.S.A. 80, 2385-2389.
74. Somogyi P., Hodgson A. J., Smith A. D., Nunzi M. G., Gorio A. and Wu J.-Y. (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin-or cholecystokinin-immunoreactive material. J. Neurosci. 10, 2590-2603.
75. Spreafico R., DeBiasi S., Frassoni C. and Battaglia G. (1988) A comparison of GAD- and GABA-immunoreactive neurons in the first somatosensory area (SI) of the rat cortex. Brain Res. 474, 192-196.
76. Thompson F. J., Fernandez J., Asanuma H. and Kubota K. (1973) Relationship between 3a sensory cortex and motor cortex in the cat. Fedn Proc. 32, 340.
77. Thompson W. D., Stoney S. D. Jr and Asanuma H. (1970) Characteristics of projections from primary sensory cortex to motorsensory cortex in cats. Brain Res. 22, 15-27.
78. Turman A. B., Ferrington D. G., Ghosh S., Morley J. W. and Rowe M. J. (1992) Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons. J. Neurophysiol. 67, 411-429.
79. Winfield D. A., Brooke R. N. L., Slope J. J. and Powell T. P. S. (1981) A combined Golgi-electron microscopic study of the synapses made by proximal axon and recurrent collaterals of a pyramidal cell in the somatic sensory cortex of the monkey. Neuroscience 6, 1217-1230.
80. Záborszky L. and Heimer L. (1989) Combination of tracer techniques, especially HRP and PHA-L, with transmitter identification for correlated light and electron microscopic studies. In Neuroanatomical Tract-Tracing Methods 2 (eds Heimer L. and Záborszky L.), pp. 49-97. Plenum, New York.