Parvalbumin is expressed in a reciprocal circuit linking the medial geniculate body and auditory neocortex in the rabbit

Journal of Comparative Neurology

Volumn 400, Issue 3, 1998, Pages 349-362

  De Venecia, Ronald K ^a   Smelser, Chad B ^a   McMullen, Nathaniel T ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Auditory system; Calcium binding proteins; Hearing; Thalamus

Indexed keywords

BIOCYTIN; BIOTIN; CALCIUM BINDING PROTEIN; DEXTRAN DERIVATIVE; PARVALBUMIN; TRACER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; INTERNEURON; MEDIAL GENICULATE BODY; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RABBIT; THALAMOCORTICAL TRACT;

ANIMALS; AUDITORY CORTEX; CALCIUM-BINDING PROTEINS; CELL SIZE; FLUORESCENT ANTIBODY TECHNIQUE; GENICULATE BODIES; NEOCORTEX; NEURONS, AFFERENT; PARVALBUMINS; PYRAMIDAL CELLS; RABBITS; THALAMUS;

EID: 0032569608     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19981026)400:3<349::AID-CNE5>3.0.CO;2-8     Document Type: Article

References (76)

1. Adams, J.C. (1981) Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29:775.
2. Andersen, R.A., P.L. Knight, and M.M. Merzenich (1980a) Thalamocortical and corticothalamic connections of AI, AII and the anterior auditory field (AAF) in the cat. Evidence for two largely segregated systems of connections. J. Comp. Neurol. 194:663-701.
3. Bajo, V.M., E.M. Rouiller, E. Welker, S. Clarke, A.E.P. Villa, Y. de Ribaupierre, and F. de Ribaupierre (1995) Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex. Hearing Res. 83:161-174.
4. Bullier, J. and G.H. Henry (1979) Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. J. Neurophysiol. 42:1271-1282.
5. Calford, M.B. and L.M. Aitkin (1983) Ascending projections to the medial geniculate body of the cat: Evidence for multiple, parallel auditory pathways through the thalamus. J. Neurosci. 3:2365-2380.
6. Campbell, M.J. and D.N. Pandya (1994) Medial geniculate body chemoarchitectonic subdivisions. Soc. Neurosci. Abstr. 20:977.
7. Celio, M.R. (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231:995-996.
8. Celio, M.R., W. Baier, L. Schärer, P.A. de Viragh, and C.H. Gerday (1988) Monoclonal antibodies directed against the calcium-binding protein parvalbumin. Cell Calcium 9:81-86.
9. DeFelipe, J., S.H.C. Hendry, and E.G. Jones (1989) Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc. Natl. Acad. Sci. USA 86:2093-2097.
10. DeFelipe, J. and E.G. Jones (1991) Parvalbumin immunoreactivity reveals layer IV of monkey cerebral cortex as a mosaic of microzones of thalamic afferent terminations. Brain Res. 562:39-47.
11. de Ribaupierre, F. (1995) Acoustical information processing in the auditory thalamus and cerebral cortex. In G. Ehret and R. Romand (eds): The Central Auditory System. New York: Oxford Press, pp. 317-397.
12. de Venecia, R.K. and N.T. McMullen (1994) Single thalamocortical axons diverge to multiple patches in neonatal auditory cortex. Dev. Brain Res. 81:135-142.
13. de Venecia, R.K., C.B. Smelser, and N.T. McMullen (1995a) Parvalbumin is expressed in a reciprocal pathway linking the medial geniculate body and auditory cortex. Soc. Neurosci. Abstr. 21:675.
14. de Venecia, R.K., C.B. Smelser, S.D. Lossmann, and N.T. McMullen (1995b) Complementary expression of parvalbumin and calbindin D-28k delineates subdivisions of the rabbit medial geniculate body. J. Comp. Neurol. 359:595-612.
15. Diamond, I.T., D. Fitzpatrick, and D. Schmechel (1993) Calcium binding proteins distinguish large and small cells of the ventral posterior and lateral geniculate nuclei of the prosimian galago and the tree shrew (Tupaia belangeri). Proc. Natl. Acad. Sci. USA90:1425-1429.
16. Gilbert, C.D. and J.P. Kelly (1975) Projections of cells in different layers of the cat's visual cortex. J. Comp. Neurol. 163:81-106.
17. Gilbert, C.D. (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J. Physiol. (Lond.) 268:391-421.
18. Harvey, A.R. (1978) Characteristics of corticothalamic neurons in area 17 of the cat. Neurosci. Let. 7:177-181.
19. Hashikawa, T., E. Rausell, M. Molinari, and E.G. Jones (1991) Parvalbumin-and calbindin-containing neurons in the monkey medial geniculate complex: Differential distribution and cortical lamina specific projections. Brain Res. 544:335-341.
20. Hashikawa, T., M. Molinari, E. Rausell, and E.G. Jones (1995) Patchy and laminar terminations of medial geniculate axons in monkey auditory cortex. J. Comp. Neurol., 362:195-208.
21. Hendry, S.H.C. and E.G. Jones (1983) The organization of pyramidal and non-pyramidal cell dendrites in relation to thalamic afferent terminations in the monkey somatic sensory cortex. J. Neurocytol. 12:227-298.
22. Hendry, S.H.C., E.G. Jones, P.C. Emson, D.E.M. Lawson, C.W. Heizman, and P. Streit (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp. Brain Res. 76:467-472.
23. Hendry, S.H.C., L.M. Kitzes, and M.N. Semple (1990) Chemical identification of physiologically characterized monkey AI cortex. Soc. Neurosci. Abstr. 16:717.
24. Hendry, S.H.C. and E.G. Jones (1991) GABA neuronal subpopulations in cat primary auditory cortex: Co-localization with calcium binding proteins. Brain Res. 543:45-55.
25. Hersch, S.M. and E.L. White (1981a) Thalamocortical synapses with corticothalamic projection neurons in mouse SmI Cortex: Electron microscopic demonstration of a monosynaptic feedback loop. Neurosci. Lett. 24:207-210.
26. Jacobson, S. and J.Q. Trojanowski (1975) Corticothalamic neurons and thalamocortical terminal fields: An investigation in rat using horseradish peroxidase and autoradiography. Brain Res. 85:385-401.
27. 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.
28. Johnson, J.K. and V.A. Casagrande (1995) Distribution of calcium-binding proteins within the parallel visual pathways of a primate (Galago crassicaudatus). J. Comp. Neurol. 356:238-260.
29. Jones, E.G. (1984) Laminar distribution of cortical efferent cells. In A. Peters and E.G. Jones (eds): Cerebral Cortex, Vol. 1. New York: Plenum, pp. 521-553.
30. Jones, E.G. and S.P. Wise (1977) Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys. J. Comp. Neurol. 175:391-438.
31. Jones, E.G. and S.H.C. Hendry (1989) Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur. J. Neurosci. 1:222-246.
32. Jones, E.G., M.E. Dell'Anna, M. Molinari, E. Rausell, and T. Hashikawa (1995) Subdivisions of macaque monkey auditory cortex revealed by calcium-binding protein immunoreactivity. J. Comp. Neurol. 362:153-170.
33. Katz, L.C. (1987) Local circuitry of identified projection neurons in cat visual cortex brain slices. J. Neurosci. 7:1223-1249.
34. Kawaguchi, Y., H. Katsumaru, T. Kosaka, C.W. Heizmann, and K. Hama (1987) Fast spiking cells in rat hippocampus (CA 1 regions) contain the calcium binding protein parvalbumin. Brain Res. 416:369-374.
35. Kawaguchi, Y. and K. Kubota (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin-and calbindin D28k-immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70:387-396.
36. Kelly J.P. and D. Wong (1981) Laminar connections of the cat's auditory cortex. Brain Res. 212:1-15.
37. King, M.A., P.M. Lewis, B.E. Hunter, and O.W. Walker (1989) Biocytin: A versatile anterograde neuroanatomical tract-tracing alternative. Brain Res. 497:361-367.
38. Kisvarday, Z.F., K.A.C. Martin, M.J. Friedlander, and P. Somogyi (1987) Evidence for interlaminar inhibitory circuits in the striate cortex of the cat. J. Comp. Neurol. 260:1-19.
39. Lewis, D.A. and J.S. Lund (1990) Heterogeneity of chandelier neurons in monkey neocortex: Corticotropin-releasing factor and parvalbumin immunoreactive populations. J. Comp. Neurol. 293:599-615.
40. Lund, J.S., R.D. Lund, A.E. Hendrikson, A.H. Bunt, and A.F. Fuchs (1975) The origin of the efferent pathways from the visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 164:287-303.
41. McMullen, N.T. and E.M. Glaser (1982) Tonotopic organization of the rabbit auditory cortex. Exp. Neurol. 75:208-220.
42. McMullen, N.T. and R.K. de Venecia (1993) Thalamocortical patches in auditory neocortex. Brain Res. 620:317-322.
43. McMullen, N.T., C.B. Smelser, and R.K. de Venecia (1994a) A quantitative analysis of parvalbumin neurons in rabbit auditory cortex. J. Comp. Neurol. 349:493-511.
44. McMullen, N.T., C.B. Smelser, and F.L.Rice (1994b) Parvalbumin expression reveals a vibrissa-related pattern in rabbit SI cortex. Brain Res. 660:225-231.
45. Mitani,A. and M. Shimokouchi (1985) Neuronal connections in the primary auditory cortex: An electrophysiological study in the cat. J. Comp. Neurol. 235:417-429.
46. Mitani, A., M. Shimokouchi, K. Itoh, S. Nomura, M. Kudo, and N. Mizuno (1985) Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. J. Comp. Neurol. 235:430-447.
47. Molinari, M., M.E. Dell'Anna, E. Rausell, M.G. Leggio, T. Hashikawa, and E.G. Jones (1995) Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity. J. Comp. Neurol., 362:171-194.
48. Morest, D.K. (1964) The neuronal architecture of the medial geniculate body of the cat. J. Anat. (Lond.) 98:611-630.
49. Morest, D.K. (1965) The laminar structure of the medial geniculate body of the cat. J. Anat. (Lond.) 99:143-160.
50. Morino-Wannier, P., S.C. Fujita, and E.G. Jones (1992) GABAergic neuronal populations in monkey primary auditory cortex denned by co-localized calcium binding proteins and surface antigens. Exp. Brain Res. 88:422-432.
51. Preuss, T.M. and J.H. Kaas (1996) Parvalbumin-like immunoreactivity of layer V pyramidal cells in the motor and somatosensory cortex of adult primates. Brain Res. 712:353-357.
52. Rausell, E. and E.G. Jones (1991a) Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex. J. Neurosci. 11:226-237.
53. Rausell, E. and E.G. Jones (1991b) Histoehemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map. J. Neurosti. 11:210-225.
54. Ravizza R.J., R.B. Straw, and P.D. Long (1976) Laminar origin of efferent projections from auditory cortex in the Golden Syrian Hamster. Brain Res. 114:497-500.
55. Robson, J.A. and W.C. Hall (1975) Connections of layer VI in striate cortex of the grey squirrel (Sciurus carolinensis). Brain Res. 93:133-130.
56. Rouiller, E.M. (1995) Functional organization of the auditory pathways. In G. Ehret and R. Romand (Eds.) The Central Auditory System, New York: Oxford Press, pp. 3-96.
57. Rouiller, E.M. and F. de Ribaupierre (1985) Origins of afferents to physiologically defined regions of the medial geniculate body of the cat: Ventral and dorsal divisions. Hearing Res. 19:97-114.
58. Rouiller, E.M. and F. de Ribaupierre (1990) Arborization of corticothalamic axons in the auditory thalamus of the cat: A PHA-L tracing study. Neurosci. Lett. 108:29-35.
59. Rouiller, E.M. and E. Welker (1991) Morphology of corticothalamic terminals arising from the auditory cortex of the rat: A Phaseolus vulgarisleucoagglutinin (PHA-L) tracing study. Hearing Res. 56:179-190.
60. Ryugo, D.K. and N.W. Weinberger (1976) Corticofugal modulation of the medical geniculate body. Exp. Neurol. 51:377-391.
61. Somogyi, P. and I. Soltész (1986) Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience 19:1051-1065.
62. Spatz, W.B., R.-B. Illing, and D.M.V. Weisenhorn (1994) Distribution of cytochrome oxidase and parvalbumin in the primary visual cortex of the adult and neonate monkey, Callithrixjacchus. J. Comp. Neurol. 339:519-534.
63. Stichel, C.C., W. Singer, C.W. Heizmann, and A.W. Norman (1987) Immunohistochemical localization of calcium-binding proteins, parvalbumin and calbindin-D 28k, in the adult and developing visual cortex of cats: A light and electron microscopic study. J. Comp. Neurol. 262:563-577.
64. Taha, S., B. Bonham, S. W. Wong, and C. Schreiner (1996) Intracortical inhibitory connections refine the specificity of cat AI neuron responsivity. Soc. Neurosci. Abstr. 22:1068.
65. Van Brederode, J.F.M., K.A. Mulligan, and A.E. Hendrickson (1990) Calcium-binding proteins as markers for subpopulations of GABAergie neurons in monkey striate cortex. J. Comp. Neurol. 298:1-22.
66. Van Brederode, J.F.M., M.K. Helliesen, and A.E. Hendrickson (1991) Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat. Neuroscience 44:157-171.
67. Vater, M. and K. Braun (1994) Parvalbumin, calbindin D-28k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats. J. Comp. Neurol. 341:534-558.
68. Veenman, L.C., A. Reiner, and M.G. Honig (1992) Biotinylated dextran amine as an anterograde tracer for single and double labeling studies. J. Neurosci. Methods 41:239-254.
69. Villa, A.E.P., E.M. Rouiller, G.M. Simm, P. Zurita, Y. de Ribaupierre, and F. de Ribaupierre (1991) Corticofugal modulation of the information processing in the auditory thalamus of the cat. Exp. Brain Res. 86:506-517.
70. Wallace, M.N., L.M. Kitzes, and E.G. Jones (1991) Chemoarchitectonic organization of the cat primary auditory cortex. Exp. Brain Res. 86:518-526.
71. Watanbe, T., K. Yanagisawa, J. Kanzaki, and Y. Katsuki (1966) Cortical efferent flow influencing unit responses of the medial geniculate body to sound stimulation. Exp. Brain Res. 2:302-317.
72. White, E.L. (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Structure Function and Theory. Boston: Birkhauser.
73. Wise, S.P. and E.G. Jones (1977) Cells of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J. Comp. Neurol. 175:129-158.
74. Wong, D. and J.P. Kelly (1981) Differentially projecting cells in individual layers of the auditory cortex: A double-labeling study. Brain Res. 230:362-366.
75. Wouterlood, F.G., W. Härtig, G. Bruckner, and M.P. Witter (1995) Parvalbumin-immunoreactive neurons in the entorhinal cortex of the rat: Localization, morphology, connectivity and ultrastructure. J. Neurocytol. 24:135-153.
76. Zhang, Y, N. Suga, and J. Yan (1997) Corticofugal modulation of frequency processing in bat auditory system. Nature. 387:900-903.