GABAergic neurons in the rat dentate gyrus are innervated by subcortical calretinin-containing afferents

Journal of Comparative Neurology

Volumn 364, Issue 3, 1996, Pages 425-438

  Nitsch, Robert ^a   Leranth, Csaba ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

calbindin; calcium binding protein; feed forward inhibition; parvalbumin; supramammillary nucleus

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTRON MICROSCOPY; FEMALE; GABAERGIC SYSTEM; IMMUNOHISTOCHEMISTRY; INNERVATION; MALE; MICROSCOPY; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; RAT; SENSORY NERVE;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBRAL CORTEX; DENTATE GYRUS; EYE PROTEINS; FEMALE; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; NERVE FIBERS; NERVE TISSUE PROTEINS; NEURONS; NEURONS, AFFERENT; PARVALBUMINS; RATS; RATS, SPRAGUE-DAWLEY; WHEAT GERM AGGLUTININ-HORSERADISH PEROXIDASE CONJUGATE;

EID: 0030044450     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960115)364:3<425::AID-CNE4>3.0.CO;2-6     Document Type: Article

References (60)

1. Amaral, D.G., and M.P. Witter (1995) Hippocampal formation. In G. Paxinos (ed.): The Rat Nervous System, 2nd Ed. New York: Academic Press, pp. 443-486.
2. Bland, B.H. (1986) The physiology and pharmacology of hippocampal formation theta rhythm. Prog. Neurobiol. 26:1-54.
3. Cajal, S.R.Y. (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés. Paris: A. Maloine.
4. Carre, G.P., and C.W. Harley (1991) Population spike facilitation in the dentate gyrus following glutamate to the lateral supramammillary nucleus. Brain Res. 568:307-310.
5. Crowne, D.P., and D.D. Radcliffe (1975) Some characteristics and functional relations of the electrical activity of the primate hippocampus and a hypothesis of hippocampal function. In R.L. Isaacson and K.H. Pribram (eds.): The Hippocampus, Vol. 2.: Neurophysiology and Behavior. New York: Plenum Press, pp. 185-206.
6. Dahl, D., and J. Winson (1986) Influence of neurons of the parafascicular region on neuronal transmission from perforant path through dentate gyrus. Brain Res. 377:211-219.
7. Deller, T., and R. Nitsch (1995) Selective rostral transection of the fornix that spares the hippocampal commissural pathway in the rat: A PHAL-tracing study. Exp. Brain Res. 104:243-248.
8. Deller, T., R. Nitsch, and M. Frotscher (1995) Phaseolus vulgaris-leucoagglutinin tracing of commissural fibers to the rat dentate gyrus: Evidence for a previously unknown commissural projection to the outer molecular layer. J. Comp. Neurol. 352:55-68.
9. Eccles, J.C. (1964) The Physiology of Synapses. Heidelberg: Springer.
10. Freund, T.F. (1989) GABAergic septo-hippocampal neurons contain parvalbumin. Brain Res. 478:375-381.
11. Freund, T.F., and M. Antal (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173.
12. Freund, T.F., G. Buzsâki, A. Leon, K.G. Baimbridge, and P. Somogyi (1990) Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Exp. Brain Res. 83:55-66.
13. Gall, C., and L. Selawski (1984) Supramammillary afferents to guinea pig hippocampus contain substance P-like immunoreactivity. Neurosci. Lett. 51:171-176.
14. Gulyás, A.I., R. Miettinen, D.M. Jacobowitz, and T.F. Freund (1992) Calretinin is present in nonpyramidal cells of the rat hippocampus. I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48:1-27.
15. Halasy, K., and P. Somogyi (1993) Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5:411-429.
16. Han, Z.S., E.H. Buhl, Z. Lörinczi, and P. Somogyi (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5:395-410.
17. Hodgson, A.J., B. Penke, A. Erdei, I.V. Chubb, and P. Somogyi (1985) Antisera to gamma aminobutyric acid. Production and characterization using a new model system. J. Histochem. Cytochem. 33:229-239.
18. Horvath, T.L., F. Naftolin, and C. Leranth (1992) Beta-endorphin innervation of dopamine neurons in the rat hypothalamus: A light and electron microscopic double immunostaining study. Endocrinology 131:1547-1555.
19. Hsu, S.M., L. Raine, and H. Fanger (1981) The use of avidin-biotinperoxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (peroxidase) procedures. J. Histochem. Cytochem. 29:577-590.
20. Ino, T., K. Itoh, T. Sugimoto, T. Kaneko, H. Kamiya, and N. Mizuno (1988) The supramammillary region of the cat sends substance P-like immunoreactive axons to the hippocampal formation and the entorhinal cortex. Neurosci. Lett. 90:259-264.
21. Jakab, R.J., and C. Leranth (1995) Septum. In G. Paxinos (ed.): The Rat Brain. New York: Academic Press, pp. 405-431.
22. Katsumaru, H., T. Kosaka, C.W. Heizmann, and K. Hama (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp. Brain Res. 72:347-362.
23. Kawaguchi, Y., H. Katsumaru, T. Kosaka, C.W. Heizmann, and K. Hama (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416:369-374.
24. Kitt, C.A., S.J. Mitchell, M.R. DeLong, B.H. Wainer, and L.D. Price (1987) Fiber pathways of basal forebrain cholinergic neurons in monkeys. Brain Res. 406:192-206.
25. Kocsis, B., and R.P. Vertes (1994) Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J. Neurosci. 14:7040-7052.
26. Kosaka, T., and K. Hama (1986) Three-dimensional structure of astrocytes in the rat dentate gyrus. J. Comp. Neurol. 249:242-260.
27. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res. 419:119-130.
28. Laurberg, S., and K.E. Soerensen (1981) Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res. 212:287-300.
29. Leranth, C., and R. Nitsch (1994) Morphological evidence that hypothalamic substance P-containing afferents are capable of filtering the signal flow in the monkey hippocampal formation. J. Neurosci. 14:4079-4086.
30. Leranth, C., and V. Pickel (1989) Electron microscopic double immunostaining methods. In L. Heimer and L. Zaborszky (eds.): Neuroanatomical Tract-Tracing Techniques II. Recent Progress. New York: Plenum Press, pp. 129-172.
31. Leranth, C., and C.E. Ribak (1991) Calcium-binding proteins are concentrated in the CA2 fields of the monkey hippocampus: A possible key to this regions resistance to epileptic damage. Exp. Brain Res. 85:129-136.
32. Lübbers, K., and M. Frotscher (1987) Fine structure and synaptic connections of identified neurons in the rat fascia dentata. Anat. Embrvol. 177:1-14.
33. Maglóczky, Z., L. Acsády, and T.F. Freund (1994) Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4:322-334.
34. Miettinen, R., A.I. Gulyás, K.G. Baimbridge, D.M. Jacobowitz, and T.F. Freund (1992) Calretinin is present in nonpyramidal cells of the rat hippocampus. II. Coexistence with other calcium-binding proteins and GABA. Neuroscience 48:29-43.
35. Mizumori, S.J., B.L. McNaughton, and C.A. Barnes (1989) A comparison of supramammillary and medial septal influences on hippocampal field potentials and single-unit activity. J. Neurophysiol. 61:15-31.
36. Nicoll, R.A., C. Schenker, and S.E. Leeman (1980) Substance P as a transmitter candidate. Annu. Rev. Neurosci. 2:227-268.
37. Nitsch, R., and C. Leranth (1993) Calretinin immunoreactivity in the monkey hippocampal formation-II. Intrinsic GABAergic and hypothalamic nonGABAergic systems. An experimental tracing and coexistence study. Neuroscience 55:797-812.
38. Nitsch, R., and C. Leranth (1994) Substance P-containing hypothalamic afferents to the monkey hippocampus: An immunocytochemical, tracing, and coexistence study. Exp. Brain Res. 101:231-240.
39. Nitsch, R., E. Soriano, and M. Frotscher (1990) The parvalbumin-containing nonpyramidal neurons in the rat hippocampus. Anat. Embryol. 181:413-425.
40. Pasquier, D.A., and F. Reinoso-Suarez (1976) Direct projections from the hypothalamus to hippocampus in the rat demonstrated by retrograde transport of horseradish peroxidase. Brain Res. 108:165-169.
41. Pasquier, D.A., and F. Reinoso-Suarez (1978) The topographic organization of hypothalamic and brainstem projections to the hippocampus. Brain Res. Bull. 3:373-389.
42. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. London: Academic Press.
43. Resibois, A., and J.H. Rogers (1992) Calretinin in rat brain: An immunohistochemical study. Neuroscience 46:101-134.
44. Ribak, C.E., L. Seress, G.M. Peterson, K.B. Seroogy, J.H. Fallon, and L.C. Schmued (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. J. Neurosci. 6:3492-3498.
45. Riley, J.H., and R.Y. Moore (1981) Diencephalic and brainstem afferents to the hippocampal formation in the rat. Brain Res. Bull. 6:437-444.
46. Rogers, J.H. (1989) Immunoreactivity for Calretinin and other calcium-binding proteins in cerebellum. Neuroscience 31:711-721.
47. Segal, M. (1979) A potent inhibitory monosynaptic hypothalamo-hippocampal connection. Brain Res. 162:137-141.
48. Seress, L., and C.E. Ribak (1985) A combined Golgi-electron microscopic study of nonpyramidal neurons in the CA 1 area of the hippocampus. J. Neurocytol. 14:717-730.
49. Seress, L., A.I. Gulyás, and T.F. Freund (1991) Parvalbumin- and CB D28k-immunoreactive neurons in the hippocampal formation of the macaque monkey. J. Comp. Neurol. 313:162-177.
50. 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.
51. Soriano, E., R. Nitsch, and M. Frotscher (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochemical studies. J. Comp. Neurol. 293:1-25.
52. Stanfield, B.B., and W.M. Cowan (1984) An EM autoradiographic study of the hypothalamo-hippocampal projection. Brain Res. 309:299-307.
53. Stewart, M., and S.E. Fox (1989a) Monkeys have hippocampal theta activity. Soc. Neurosci. Abstr. 15:1250
54. Stewart, M., and S.E. Fox (1989b) Do septal neurons pace the hippocampal theta rhythm?. Trends Neurosci. 13:163-168.
55. Tóth, K., and T.F. Freund (1992) CB D28k-containing nonpyramidal cells in the rat hippocampus: Their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
56. Vertes, R.P. (1992) PHA-L analysis of projections from the supramammillary nucleus in the rat. J. Comp. Neurol. 326:595-622.
57. Wouterlood, F.G., E. Saldana, and M.P. Witter (1990) Projection from the nucleus reuniens thalami to the hippocampal region: Light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 296:179-203.
58. Wyss, J.M., L.W. Swanson, and W.M. Cowan (1979a) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463-476.
59. Wyss, J.M., L.W. Swanson, and W.M. Cowan (1979b) Evidence for an input to the molecular layer and the stratum granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat. Embryol. 156:165-176.
60. Yanagihara, M., and K. Niimi (1988) Substance P-like immunoreactive projection of the hippocampal formation from the posterior hypothalamus in the cat. Brain Res. Bull. 22:689-694.