The entorhino-septo-supramammillary nucleus connection in the rat: Morphological basis of a feedback mechanism regulating hippocampal theta rhythm

Neuroscience

Volumn 88, Issue 3, 1999, Pages 701-718

  Leranth, C ^a   Carpi, D ^b   Buzsaki, G ^b   Kiss, J ^c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

Author keywords

3H D aspartate; Antero and retrograde tracing; Calretinin; Co localization; GABA

Indexed keywords

CALRETININ; DEXTRO ASPARTIC ACID; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; FEEDBACK SYSTEM; FEMALE; GABAERGIC TRANSMISSION; HIPPOCAMPUS THETA RHYTHM; IMMUNOHISTOCHEMISTRY; ISOTOPE LABELING; LIMBIC SYSTEM; MALE; MAMMILLARY BODY; NERVE PROJECTION; NERVE TRACT; NEUROCHEMISTRY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SEPTUM NUCLEUS; TISSUE DISTRIBUTION;

ANIMALS; ASPARTIC ACID; AXONAL TRANSPORT; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; ENTORHINAL CORTEX; FEEDBACK; FEMALE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MALE; MAMILLARY BODIES; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEURONS; PHYTOHEMAGGLUTININS; RATS; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI; THETA RHYTHM;

EID: 0032890426     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00245-0     Document Type: Article

References (48)

1. Alonso A., Khateb A., Fort P., Jones B. E. and Muhlethaler M. (1996) Differential oscillatory properties of cholinergic and noncholinergic nucleus basalis neurons in guinea pig brain slice. Eur. J. Neurosci. 8, 169-182.
2. Alonso A. and Garcia-Austt E. (1987) Neuronal structures of theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Expl Brain Res. 67, 502-509.
3. Alonso A. and Kohler C. (1984) A study of the reciprocal connections between the septum and entorhinal area using anterograde and retrograde axonal transport methods in the rat brain. J. comp. Neurol. 225, 327-343.
4. Amaral D. G. and Witter M. P. (1995) Hippocampal formation. In The Rat Nervous System (ed. Paxinos G.), pp. 443-493. Academic, San Diego.
5. Arnolds D. E., Aitink J. W., Boeyinga P. and Lopes de Silvia F. H. (1979) Hippocampal EEG in dog, cat, and man. Rev. Electroenceph. Neurophysiol. Clin. 9, 326-332.
6. Barrenechea C., Pedemonte M., Nunez A. and Garcia-Austt E. (1995) In vivo intracellular recording of medial septal and diagonal band of Broca neurons: relationships with theta rhythm. Expl Brain Res. 103, 31-40.
7. Bland B. H., Konopacky J., Kirk I. J., Oddie S. D. and Dickson C. T. (1995) Discharge patterns of hippocampal theta-related cells in the caudal diencephalon. J. Neurophysiol. 74, 322-333.
8. Borhegyi Z. and Leranth C. (1997) Distinct substance P- and calretinin-containing projections from the supramammillary area to the hippocampus in rats; a species difference between rats and monkeys. Expl Brain Res. 115, 369-374.
9. Borhegyi Z., Maglóczky Z., Acsady L. and Freund T. F. (1998) The supramammillary nucleus innervates cholinergic and GABAergic neurons in the medial septum-diagonal band of Broca complex. Neuroscience 82, 1053-1065.
10. Buzsaki G., Leung L. W. and Vanderwolf C. H. (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287, 139-171.
11. Carpi D., Sik A. and Buzsaki G. (1995) Activity of nucleus triangularis septi (TS) neurons to theta and sharp waves in the behaving rat. Society for Neuroscience Annual Meeting 2, 1206, San Diego.
12. Eccles J. C. (1964) The Physiology of Synapses. Springer, Heidelberg.
13. Grastyan E., Lissak K., Madarasz I. and Donhoffer H. (1959) The hippocampal electric activity during the development of conditioned reflexes. Electroenceph. clin. Neurophysiol. 11, 409-430.
14. Hodgson A. J., Penke B., Erdei A., Chub I. V. and Somogyi P. (1985) Antisera to gamma aminobutyric acid. Production and characterization using a new model system. J. Histochem. Cytochem. 33, 229-239.
15. Holderith N., Varoqueaux F., Borhegyi Z. and Leranth C. (1998) Dual (excitatory and inhibitory) calretinin innervation of AMPA receptor-containing neurons in the lateral septum. Expl Brain Res. 119, 65-72.
16. Jakab R. L. and Leranth C. (1994) Septum. In The Rat Nervous System (ed. Paxinos G.), pp. 405-442. Academic, San Diego.
17. Kirk I. J. and McNaughton N. (1991) Supramammillary cell firing and hippocampal rhythmical slow activity. NeuroReport 2, 723-725.
18. Kirk I. J. and McNaughton N. (1993) Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activity. Hippocampus 3, 517-529.
19. Kiss J., Maglóczky Z., Somogyi J. and Freund T. F. (1997) Distribution of calretinin-containing neurons relative to other neurochemically identified cell types in the medial septum of the rat. Neuroscience 78, 399-410.
20. Kocsis B. and Vertes R. P. (1992) Dorsal raphe neurons: synchronous discharge with the theta rhythm of the hippocampus in the freely behaving rat. J. Neurophysiol. 68, 1463-1467.
21. Kocsis B. and Vertes R. P. (1994) Characterization of neurons of the supramammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J. Neurosci. 4, 7040-7052.
22. Kosaka T., Kosaka K., Tateishi K., Hamaoka Y., Yamaihara M., Wu J. Y. and Hama K. (1985) GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J. comp. Neurol. 239, 420-430.
23. Krieg W. J. S. (1946) Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas. J. comp. Neurol. 84, 221-275.
24. Krieg W. J. S. (1946) Connections of the cerebral cortex. II. The albino rat. B. Structure af the cortical areas. J. comp. Neurol. 84, 277-323.
25. Lee M. G., Chrobak J. J., Sik A., Wiley R. G. and Buzsaki G. (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62, 1033-1047.
26. Leranth C. and Kiss J. (1996) A population of supramammillary area calretinin neurons terminating on medial septal area cholinergic and lateral septal area calbindin-containing cells are aspartate/glutamatergic. J. Neurosci. 16, 7699-7710.
27. Leranth C. and Nitsch R. (1994) Hypothalamic substance P-containing afferents can filter the signal flow in the monkey hippocampal formation: morphological evidence for stimulation and feed-forward inhibition of different populations of granule cells and indirect inhibition of CA3 pyramidal neurons. J. Neurosci. 14, 4079-4094.
28. Maglóczky Z., Acsady L. and Freund T. F. (1994) Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4, 322-334.
29. McNaughton N., Logan B., Panickar K. S., Kirk I. J., Pan W. X., Brown N. T. and Heenan A. (1995) Contribution of synapses in the medial supramammillary nucleus to the frequency of hippocampal theta rhythm in freely moving rats. Hippocampus 5, 534-545.
30. Miettinen M., Pitkãnen A. and Miettinen R. (1997) Distribution of calretinin-immunoreactivity in the rat entorhinal cortex: coexistence with GABA. J. comp. Neurol. 378, 363-378.
31. Mitchell S. J. and Ranck J. B. (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res. 189, 49-66.
32. Nitsch R. and Leranth C. (1996) GABAergic neurons in the rat dentate gyrus are innervated by subcortical calretinin-containing afferents. J. comp. Neurol. 364, 425-438.
33. Oertel W. H., Schmechel D. E., Mugnaini E., Tappaz M. L. and Kopin I. J. (1982) Immunohistochemical localization of glutamate decarboxylase in the rat cerebellum with a new antiserum. Neuroscience 6, 2715-2735.
34. Pare D. and Gaudreau H. (1996) Projection cells and interneurons of the lateral and basolateral amygdala: distinct firing patterns and differential relation to theta and delta rhythms in conscious cats. J. Neurosci. 16, 3334-3350.
35. Petsche H., Stumpf C. and Gogolak G. (1962) Medial septum as a pacemaker of hippocampal theta waves. Electroenceph. clin. Neurophysiol. 14, 202-211.
36. Risold P. Y. and Swanson L. W. (1996) Structural evidence for functional domains in the rat hippocampus. Science 272, 1484-1486.
37. Rogers J. H. (1987) Calretinin: a gene for novel calcium-binding protein expressed principally in neurons. J. Cell Biol. 105, 1343-1353.
38. Somogyi P. and Hodgson A. J. (1985) Antisera to gamma-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.
39. Stewart M. and Fox S. E. (1989) Firing relations of medial septal neurons to the hippocampal theta rhythm in urethane anesthetized rats. Expl Brain Res. 77, 507-516.
40. Stewart M. and Fox S. E. (1989) Two populations of rhythmically bursting neurons in rat medial septum are revealed by atropine. J. Neurophysiol. 61, 982-993.
41. Stewart M. and Fox S. E. (1990) Firing relations of lateral septal neurons to the hippocampal theta rhythm in urethane anesthetized rats. Expl Brain Res. 79, 92-96.
42. Stewart M. and Fox S. E. (1991) Hippocampal theta activity in monkeys. Brain Res. 538, 59-63.
43. Swanson L. W. and Cowan W. M. (1979) The connections of the septal region of the rat. J. comp. Neurol. 186, 621-656.
44. Thinschmidt J. S., Kinney G. G. and Kocsis B. (1995) The supramammillary nucleus: is it necessary for the mediation of hippocampal theta rhythm? Neuroscience 67, 301-312.
45. Vanderwolf C. H. (1969) Hippocampal electric activity and voluntary movement in the rat. Electroenceph. clin. Neurophysiol. 26, 407-418.
46. Vertes R. P. (1986) Brainstem modulation of the hippocampus. Anatomy, physiology, and significance. In The Hippocampus (eds Isaacson R. L. and Pribram K. H.), Vol. 4, pp. 41-75. Plenum, New York.
47. Vertes R. P. (1992) PHA-L analysis of projections from the supramammillary nucleus in the rat. J. comp. Neurol. 326, 595-622.
48. Vertes R. P. and Kocsis B. (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81, 893-926.