Microcircuitry of forward and feedback connections within rat visual cortex

Journal of Comparative Neurology

Volumn 368, Issue 3, 1996, Pages 383-398

  Johnson, Randall R ^a   Burkhalter, Andreas ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

dendritic shaft; dendritic spine; GABA inhibition; synapse; visual system

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEEDBACK SYSTEM; GABAERGIC SYSTEM; IMMUNOHISTOCHEMISTRY; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; VISUAL CORTEX;

ANIMALS; DENDRITES; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MICROSCOPY, ELECTRON; PHYTOHEMAGGLUTININS; RATS; RATS, INBRED STRAINS; SENSITIVITY AND SPECIFICITY; SYNAPSES; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 0029940489     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960506)368:3<383::AID-CNE5>3.0.CO;2-1     Document Type: Article

References (100)

1. Adams, J.C. (1981) Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 2:141-145.
2. 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.
3. Agmon, A., and D.K. O'Dowd (1992) NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. J. Neurophysiol. 68:345-349.
4. Ahmed, B., J.C. Anderson, R.J. Douglas, K.A.C. Martin, and J.C. Nelson (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J. Comp. Neurol. 341:39-49.
5. Amitai, Y., A. Friedman, B.W. Connors, and M.J. Gutnick (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb. Cortex 3:26-38.
6. Anderson, J.C., R. J. Douglas, K.A.C. Martin, and J.C. Nelson (1994) Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J. Comp. Neurol. 341:25-38.
7. Artola, A., and W. Singer (1987) Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330:649-652.
8. Beaulieu, C., G. Campistron, and C. Crevier (1994) Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat. J. Comp. Neurol. 339:559-572.
9. Berman, N.J., R.J. Douglas, and K.A.C. Martin (1992) GABA-mediated inhibition in the neural networks of visual cortex. Prog. Brain Res. 90:443-476.
10. Cauller, L.J., and B.W. Connors (1992) Functions of very distal dendrites: Experimental and computational studies of layer I synapses on neocortical pyramidal cells. In T. McKenna, J. Davis, and S.F. Zornetzer (eds): Single Neuron Computation. Boston: Academic Press, pp. 199-229.
11. Cauller, L.J., and B.W. Connors (1994) Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex. J. Neurosci. 14:751-762.
12. Coggeshall, R.E. (1992) A consideration of neural counting methods. Trends Neurosci. 15:9-13.
13. Collingridge G.L., and W. Singer (1990) EAA pharmacology: Excitatory amino acid receptors and synaptic plasticity. Trends Neurosci. 11:290-295.
14. Colonnier, M. (1981) The electron-microscopic analysis of the neuronal organization of the cerebral cortex. In F.O. Schmitt, F.G. Worden, G. Adelman, and S.G. Dennis (eds): The Organization of the Cerebral Cortex. Cambridge: MIT Press, pp. 125-152.
15. B-mediated processes in visual cortex. Prog. Brain Res. 90:335-348.
16. B receptors-mediated responses in neocortex of rat and cat. J. Physiol. 406:443-468.
17. Coogan, T.A., and A. Burkhalter (1990) Conserved patterns of corticocortical connections define areal hierarchy in rat visual cortex. Exp. Brain Res. 80:49-53.
18. Coogan, T.A., and A. Burkhalter (1993) Hierarchical organization of areas in rat visual cortex. J. Neurosci. 3:3749-3772.
19. Czeiger, D., and E.L. White (1993) Synapses of extrinsic and intrinsic origin made by callosal projection neurons in mouse visual cortex. J. Comp. Neurol. 330:502-513.
20. Daw, N.W., P.S.G. Stein, and K. Fox (1993) The role of NMDA receptors in information processing. Annu. Rev. Neurosci. 16:201-222.
21. Dehay. C., R.J. Douglas, K.A.C. Martin, and C. Nelson (1991) Excitation by geniculocortical synapses is not 'vetoed' at the level of dendritic spines in cat visual cortex. J. Physiol. 440:723-734.
22. Domenici, L., G.W. Harding, and A. Burkhalter (1995) Patterns of synaptic activity in forward and feedback pathways within rat visual cortex. J. Neurophysiol. (in press).
23. Douglas, R.J., and K.A.C. Martin (1991) A functional microcircuit for cat visual cortex. J. Physiol. 440:735-769.
24. Einstein, G., and D. Fitzpatrick (1991) Distribution and morphology of area 17 neurons that project to the cat's extrastriate cortex. J. Comp. Neurol. 303:132-149.
25. Elhanany, E., and E.L. White (1990) Intrinsic circuitry: Synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J. Comp. Neurol. 291:43-54.
26. Espinoza, S.G., and H.C. Thomas (1983) Retinotopic representation of striate and extrastriate visual cortex in the hooded rat. Brain Res. 272:137-144.
27. Feldman. M.L., and A. Peters (1978) The forms of non-pyramidal neurons in the visual cortex of the rat. J, Comp. Neurol. 179:761-794.
28. Felleman. D.J., and D.C. Van Essen (1991) Distributed hierarchical processing in the primate cortex. Cereb. Cortex 1:1-47.
29. Fisken, R.A., L.J. Garey, and T.P.S. Powell (1975) The intrinsic, association and commissural connections of area 17 of the visual cortex. Philos. Trans. R. Soc. Lond. [Biol.] 272:487-536.
30. Freund, T.F., and A-I. Gulyás (1991) GABAergic interneurons containing calbindin D28K or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex. J. Comp. Neurol. 314:187-99.
31. Freund, T.F., K.A.C. Martin, I. Soltesz, P. Somogyi, and D. Whitteridge D (1989) Arborization pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey. J. Comp. Neurol. 289:315-336.
32. Freund. T.F., K.A.C. Martin, and D. Whitteridge (1985) Innervation of cat visual area 17 and 18 by physiologically identified X- and Y-type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements. J. Comp. Neurol. 242:263-274.
33. Gabbott, P.L.A., K.A.C. Martin, and D. Whitteridge (1987) Connections between pyramidal neurons in layer 5 of cat visual cortex (area 17). J. Comp. Neurol. 259:364-381.
34. Garey, L.J., and T.P.S. Powell (1971) An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proc. R. Soc. [Biol.] 179:21-40.
35. Gerfen, C.R., and P.E. Sawchenko (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons, and terminals: Imrmunocytochemical localization of an axonally transported lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res. 290:219-238.
36. Girard. P., and J. Bullier (1989) Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. J. Neurophysiol. 62:1287-1302.
37. Girard, P., P.A. Salin, and J. Bullier (1991a) Visual activity in macaque area V4 depends on area 17 input. Neuroreport 2:81-84.
38. Girard, P., P.A. Salin, and J. Bullier (1991b) Visual activity in areas V3A and V3 during reversible inactivation of area V1 in the macaque monkey. J. Neurophysiol. 66:1493-1503.
39. Gray, E.G. (1959) Axo-somatic and axo-dendritic synapses in the cerebral cortex: An electron microscopic study. J. Anat. (Lond.) 93:420-433.
40. Haenny, P.E., J.H.R, Maunsell, and P.H. Schiller (1988). State dependent activity in monkey visual cortex. Exp. Brain Res. 69:245-259.
41. Hirsch. J.A. (1995) Synaptic integration in layer IV of the ferret striate cortex. J. Physiol. 483:183-199.
42. Hirsch, J.A., and C.D. Gilbert (1991) Synaptic physiology of horizontal connections in the cat's visual cortex. J. Neurosci. 11:1800-1809.
43. Hirsch. J.A., and C.D. Gilbert (1993) Long-term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex. J. Physiol. 461:247-262.
44. Ichikawa. M., K. Arissian, and H. Asanuma (1985) Distribution of corticocortical and thalamocortical synapses on identified motor cortical neurons in the cat: Golgi, electron microscopic and degeneration study. Brain Res. 345:87-101.
45. Jiang, X., R.R. Johnson, and A. Burkhalter (1993) Visualization of dendritic morphology of cortical projection neurons by retrograde axonal tracing. J. Neurosci. Meth. 50:45-60.
46. Johnson, R.R., and A. Burkhalter (1993) Corticocortical feedback connections synapse selectively with dendritic spines. Soc. Neurosci. Abstr. 18:300.
47. Johnson, R.R., and A. Burkhalter (1994a) Evidence for excitatory amino acid neurotransmitters in forward and feedback Corticocortical pathways within rat visual cortex. Eur. J. Neurosci. 6:272-286.
48. Johnson, R.R., and A. Burkhalter (1994b) Different microcircuits for forward corticocortical and LP (pulvinar) projections in rat extrastriate visual cortex. Soc. Neurosci. Abstr. 20:427.
49. Jones. E.G., and T.P.S. Powell (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. Philos. Trans. R. Soc. Lond. [Biol.] 257:45-62.
50. Kato. N., A. Artola, and W. Singer (1991) Developmental changes in the susceptibility of long-term potentiation of neurones in rat visual cortex slices. Dev. Brain Res. 60:43-50.
51. Keller. A., and H. Asanuma (1993) Synaptic relationships involving local axon collaterals of pyramidal neurons in the cat motor cortex. J. Comp. Neurol. 336:229-242.
52. Kim, H.G., and B.W. Connors (1993) Apical dendrites of the neocortexcorrelation between sodium-dependent and calcium-dependent spiking an pyramidal cell morphology. J. Neurosci. 13:5301-3311.
53. Kirkwood. A., and M.F. Bear (1994) Hebbian synapses in visual cortex. J. Neurosci. 14:1634-1645.
54. Kisvárday, Z.F., K.A.C. Martin, D. Whitteridge, and P. Somogyi (1985) Synaptic connections of intracellularly filled clutch neurons, a type of small basket neuron in the visual cortex of the cat. J. Comp. Neurol. 241:111-137.
55. Knierim, J.J., and D.C. Van Essen (1992) Neuronal responses to static texture patterns in area Vl of the alert macaque monkey. J. Neurophysiol. 67:961-980.
56. Koch, C. (1987) The action of the corticofugal pathway on sensory thalamic nuclei: A hypothesis. Neuroscience 23:399-406.
57. Koch, C., and T. Poggio (1985) The synaptic veto mechanism: Does it underline direction and orientation selectivity in the visual cortex? In D. Rose and V.G. Dobson (eds): Models of the Visual Cortex. New York: John Wiley, pp. 408-419.
58. Komatsu, Y., K. Fujii, J. Maeda, H. Sakaguchi, and K. Toyama (1988) Long-term potentiation of synaptic transmission in kitten visual cortex. J. Neurophysiol. 59:124-141.
59. Larkman, A.U. (1991) Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J. Comp. Neurol. 306:332-13.
60. Lohmann, H., and B. Rörig (1994) Long range horizontal connections between supragranular pyramidal cells in the extrastriate visual cortex of the rat. J. Comp. Neurol. 344:543-558.
61. Lowenstein, P.R., and P. Somogyi (1991) Synaptic organization of corticocortical connections from the primary visual cortex to the posteromedial lateral suprasylvian visual area in the cat. J. Comp. Neurol. 310.253-266.
62. Luhmann, H.J., and D.A. Prince (1991) Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65:247-263.
63. Maffei, L., N. Berardi, L. Domenici, L, V. Parisi, and T. Pizzorusso (1992) Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. J. Neurosci. 12:4651-4662.
64. Maunsell. J.H.R., G. Sclar, T.A. Nealey, and D.D. DePriest (1991) Extraretinal representation in area V4 in the macaque monkey. Vis. Neurosci. 7:561-573.
65. McCormick, D.A., B.W. Connors, J.W. Lighthall, and DA. Prince (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54:782-806.
66. McDonald, C.T., and A. Burkhalter (1993) Organization of long-range inhibitory connections within rat visual cortex. J. Neurosci. 13:768-781.
67. McGuire, B.A., J.P. Hornung, C.D. Gilbert, and T.N. Wiesel (1984) Patterns of synaptic input to layer 4 of cat striate cortex. J. Neurosci. 4:3021-3033.
68. McGuire, B.A., C.D. Gilbert, P.K. Rivlin, and T.N. Wiesel (1991) Targets of horizontal connections in macaque primary visual cortex. J. Comp. Neurol. 305:370-392.
69. Miyashita, Y., S. Higuchi, X. Zhou, H. Okuno, and I. Hasegawa (1994) Disruption of backward connections from the rhinal cortex impairs visual associative coding of neurons in inferotemporal cortex of monkeys. Soc. Neurosci. Abstr. 20:428.
70. Moran, J., and R. Desimone (1985) Selective attention gates visual processing in the extrastriate cortex. Science 229:782-784.
71. Motter, B.C. (1993) Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J. Neurophysiol. 70:909-919.
72. Motter, B.C. (1994) Neural correlates of feature selective memory and pop-out in extrastriate area V4. J. Neurosci. 14:2190-2199.
73. Olshausen, B.A., C.H. Anderson, and D.C. Van Essen (1993) A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information. J. Neurosci. 13:4700-4719.
74. Peters, A. (1985) The visual cortex of the rat. In A. Peters and E.G. Jones (eds): Cerebral Cortex, Vol. 3. New York: Plenum, pp. 19-80.
75. Peters, A., and M.L. Feldman (1976) The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. I. General description. J. Neurocytol. 5:63-84.
76. Peters. A., and B.R. Payne (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb. Cortex 3:69-78.
77. Peters, A., D.A. Kara, and K.M. Harriman (1985) The neuronal composition of area 17 of rat visual cortex. III. Numerical considerations. J. Comp. Neurol. 238:263-274.
78. Peters. A., S.L. Palay, and H.D. Webster (1991) Fine Structure of the Nervous System. New York: Oxford University Press.
79. Porter, L.L. (1991) Patterns of connectivity in the cat sensory-motor cortex: A light and electron microscope analysis of the projection arising from area 3a. J. Comp. Neurol. 312:404-414.
80. Porter, L.L., and T. Sakamoto (1988) Organization and synaptic relationships of the projection from the primary sensory to the primary motor cortex in the cat. J. Comp. Neurol. 271:287-396.
81. Press, W.A., J.J. Knierim, and D.C. Van Essen (1994) Neuronal correlates of attention to texture patterns in macaque striate cortex. Soc. Neurosci. Abstr. 20:838.
82. Rockland, K.S., and K.L. Douglas (1993) Excitatory contacts of feedback connections in layer 1 of area V1: An EM-biocytin study in the macaque. Soc. Neurosci. Abstr. 19:424.
83. Sakai, K., and Y. Miyashita (1991) Neural organization for the long-term memory of paired associates. Nature 354:152-155.
84. Sandell, J.H., and P.H. Schiller (1982) Effect of cooling area 18 on striate cortex cells in the squirrel monkey. J. Neurophysiol. 48:38-48.
85. Schiller, P.H., and J.G. Malpeli (1977) The effect of striate cortex cooling on area 18 cells in the monkey. Brain Res. 126:366-369.
86. Shao, Z., G.W. Harding, and A. Burkhalter (1995) Distinct synaptic mechanisms in forward and feedback circuits within rat visual cortex. Soc. Neurosci. Abstr. 21:1274.
87. Sloper, J.J. (1973) An electron microscopic study of the termination of afferent connections to the primate motor cortex. J. Neurocytol. 2:361-368.
88. Sloper, J.J., and T.P.S. Powell (1979) An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Philos. Trans. R. Soc. Lond. [Biol.] 285:199-224.
89. Somers, D.C., S.B. Nelson, and M. Sur (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15:5448-5465.
90. A receptors in the lateral geniculate nucleus and visual cortex. In D.M. Lam and C.D. Gilbert (eds): Neural Mechanisms of Visual Perception. Woodlands, TX: Proceedings of Retina Research Foundation Symp. Vol. 2, pp. 35-62.
91. Somogyi, P., and A.J. Hodgson (1985) Antisera to γ-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of Cat striate cortex. J. Histochem. Cytochem. 33:249-257.
92. Somogyi, P., and I. Soltész (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidasefilled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19:1051-1065.
93. Somogyi, P., Z.F. Kisvárday, K.A.C. Martin, and D. Whitteridge (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261-294.
94. Sterio, D.C. (1984) The unbiased estimation of number and sizes of arbitrary particles using the dissector. J. Microsc. 134:127-136.
95. Strick, P.L., and P. Sterling (1974) Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscopy study. J. Comp. Neurol. 153.-77-106.
96. Stuart, G.J., and B. Sakmann (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69-72.
97. Thomas, H.C., and S.G. Espinoza (1987) Relationships between interhemispheric cortical connections and visual areas in hooded rats. Brain Res. 477:214-224.
98. White, E.L. (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Boston: Birkhäuser.
99. White, E.L., and D. Czeiger (1991) Synapses made by axons of callosal projection neurons in mouse somatosensory cortex: Emphasis on intrinsic connections. J. Comp. Neurol. 303:233-244.
100. White, E.L., and A. Keller (1987) Intrinsic circuitry involving the local axon collaterals of corticothalamic projection cells in mouse SmI cortex. J. Comp. Neurol. 262:13-26.