Bilateral organization of parallel and serial pathways in the dentate gyrus demonstrated by current-source density analysis in the rat

Journal of Neurophysiology

Volumn 75, Issue 1, 1996, Pages 329-342

  Golarai, Golijeh ^a   Sutula, Thomas P ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; DENTATE GYRUS; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPUS; INFORMATION PROCESSING; MALE; MEMBRANE CURRENT; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPTIC TRANSMISSION;

EID: 0030030369     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.75.1.329     Document Type: Article

References (65)

1. ACKROYD, M. H. Digital Filters. London: Butterworths, 1973.
2. AMARAL, D. G. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182: 851-914, 1978.
3. AMARAL, D. G. Synaptic extensions from the mossy fibers of the fascia dentata. Anat. Embryol. 155: 241-251, 1979.
4. AMARAL, D. G. Emerging principles of intrinsic hippocampal organization. Curr. Opin. Neurobiol. 3: 225-229, 1993.
5. AMARAL, D G., INSAUSTI, R., AND COWAN, W. M. The commissural connections of the monkey hippocampal formation. J Comp. Neurol. 224: 307-336, 1984
6. AMARAL, D. G., ISHIZUKA, N., AND CLAIBORNE, B. Neurons, numbers, and the hippocampal network. Prog. Brain Res. 83: 1-11, 1990.
7. AMARAL, D. G. AND WITTER, M. P. The three dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31: 571-591, 1989.
8. ANDERSEN, P., HOLMQUIST, B , AND VOORHOEVE, P. I. Entorhinal activation of dentate granule cells. Acta Physiol. Scand. 66: 448-460, 1966.
9. BLACKSTAD, T. W. Commissural connections of the hippocampal regionin the rat, with special reference to their mode of termination. J. Comp. Neurol. 105: 417-537, 1956.
10. BLACKSTAD, T. W. On the termination of some afferents to the hippocampus and fascia dentata. Acta Anat. 35: 202-214, 1958
11. BRECKOW, J., KALMRING, K., AND ECKHORN, R. Multichannel-recordings and real-time current source density (CSD) analysis m the central nervous system of insects. Biol. Cybern. 45: 115-121, 1982.
12. BUZSAKI, G. AND EIDELBERG, E. Commissural projections to the dentate gyrus of the rat: evidence for feed-forward inhibition. Brain Res. 230: 346-350, 1981.
13. CAIN, D. P., BOON, F., AND HARGREAVES, E. L. Evidence for different neurochemical contribution to long-term potentiation and to kindling and kindling-induced potentiation: role of NMDA and urethane-sensitive mechanisms. Exp. Neurol. 116: 330-338, 1992.
14. CLAIBORNE, B. J., AMARAL, D. G., AND COWAN, M. W. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J. Comp. Neurol. 246: 435-458, 1986.
15. DEADWYLER, S. A., WEST, J. R., COTMAN, C. W., AND LYNCH, G. S. A neurophysiological analysis of commissural projections to dentate gyrus of the rat. J. Neurophysiol. 38: 167-184, 1975.
16. DEMETER, S., ROSENE, D. L., AND VAN HOESEN, G. Interhemispheric pathways of the hippocampal formation, presubiculum, and entorhinal and posterior para-hippocampal cortices in the rhesus monkey. J. Comp. Neurol. 233: 30-47, 1985.
17. DEMETER, S., ROSENE, D. L., AND VAN HOESEN, G. Fields of origin and pathways of the interhemispheric commissures in the temporal lobe of macaques. J. Comp. Neurol. 302: 29-53, 1990.
18. DOUGLAS, R. M., MCNAUGHTON, B. L., AND GODDARD, G. Commissural inhibition and facilitation of granule cell discharge in fascia dentata. J. Comp. Neurol. 219: 285-294, 1983.
19. FREEMAN, J. A. AND NICHOLSON, C. Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 38: 369-382, 1975.
20. FRICKE, R. AND COWAN, W. M. An autoradiograhic study of the commissural and ipsilateral hippocampo-dentate projections in the adult rat. J. Comp. Neurol. 181: 253-270, 1978.
21. FRICKE, R. A AND PRINCE, D. A. Electrophysiology of dentate gyrus granule cells. J. Neurophysiol. 51: 195-209, 1984.
22. FROTSCHER, M., SERESS, L., SCHWERDTFEGER, W. K., AND BUHL, E. The mossy cells of the fascia dentata: a comparative study of their fine structure and synaptic connections in rodents and primates. J. Comp. Neurol. 312: 145-163, 1991.
23. GLUCK, M. A. AND GRANGER, R. Computational models of the neural bases of learning and memory. Annu Rev. Neurosci. 16: 667-706, 1993.
24. GOLARAI, G AND SUTULA, T. P. Parallel processing in the hippocampal formation demonstrated by in-vivo current source density analysis. Soc. Neurosci. Abstr. 147: 11, 1993.
25. GOLDOWITZ, D., WHITE, F. W., STEWARD, O., LYNCH, G., AND COTMAN, C. Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat. Exp. Neurol. 47: 433-441, 1975.
26. GOTTLIEB, D. I. AND COWAN, W. M. Autoradiographic studies of the commissural and ipsilaleral association connections of the hippocampus and dentate gyrus of the rat. I. Commissural connections. J. Comp. Neurol. 149: 393-422, 1973.
27. HABERLY, L. B. AND SUTULA, T. P. Neuronal processes that underlie expression of kindled epileptiform events in the piriform cortex in vivo. J. Neurosci. 12: 2211-2224, 1992.
28. HAGINS, W. A., PENN, R. D., AND YOSHIKAMI, S. Dark current and photocurrent in retinal rods. Biophys. J. 10: 380-412, 1970.
29. HASHEMZADEH-GARGARI, H., COLBERT, C. M., AND LEVY, W. B. Refining the temporal definition of an association at the neuronal level using long-term potentiation and long-term depression in the dentate gyrus. Neurosci. Lett. 126: 37-40, 1991.
30. KETCHUM, K. L AND HABERLY, L. B. Membrane currents evoked by afferent fiber stimulation in rat piriform cortex. I. Current source-density analysis. J Neurophysiol. 69, 248-260, 1993a
31. KETCHUM, K. L. AND HABERLY, L. B. Membrane currents evoked by afferent stimulation in rat piriform cortex. II. Analysis with a system model. J. Neurophysiol. 69: 261-281, 1993b.
32. LAURBERG, S. AND SORENSEN, K. E. Associational and Commissural collaterals of neurons m the hippocampal formation (hilus fasciae dentata and subfield CA3). Brain Res. 212: 287-300, 1981.
33. LEVY, W. B. AND STEWARD, O. Temporal contiguity requirement for long-term associative potentiation/depression in the hippocampus. Neuroscience 8: 791-797, 1983.
34. LOMO, T. Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation. Exp. Brain Res. 12: 18-45, 1971
35. LOPEZ DA SILVA, F. H., WITTER, M. P., BOEIJINGA, P. H., AND LOHMAN, A. H. M. Anatomical organization and physiology of the limbic cortex. Physiol. Rev. 70: 453-511, 1990.
36. MCNAUGHTON, B. L. AND MORRIS, R. G. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10: 408-415, 1987.
37. MISGELD, U., BIJAK, M., AND BRUNNER, H. Granule cell inhibition and the activity of hilar neurons. Epilepsy Res. 7, Suppl.: 113-118, 1992a.
38. MISGELD, U., BIJAK, M., BRUNNER, H., AND DEMBOWSKY, K. K-dependent inhibition in the dentate-CA3 network of guinea pig hippocampal slices. J. Neurophysiol. 68: 1548-1557, 1992b.
39. MISGELD, U., BUZSAKI, G., PRINCE, D. A., AND BOWERY, N. G. Blockade by (-)baclofen of recurrent inhibition in the guinea pig dentate gyrus in vitro. Epilepsy Res. 8, Suppl.: 39-45, 1992c.
40. MITZDORF, U. Justification of the assumption of constant resistivity used in current source density calculation. J. Physiol. Lond. 304: 216-220, 1980.
41. MITZDORF, U. Current source density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65: 37-100, 1985.
42. MULLER, W. AND MISGELD, U. Inhibitory role of dentate hilus neurons in guinea pig hippocampal slice. J. Neurophysiol. 64: 46-56, 1990.
43. NICHOLSON, C. Generation and analysis of extracellular field potentials. Prog. Neurobiol. 32: 93-147, 1989.
44. NICHOLSON, C. AND FREEMAN, J. A. Theory of current source density and determination of conductivity tensor for anuran cerebellum. J. Neurophysiol. 38: 356-368, 1975.
45. RIBAK, C. E., SERBSS, L., PETERSON, G. M., SEROGY, K. B., FALLON, J. H., AND SCHMUED, L. C. A GABAergic inhibitory component within the hippocampal commissural pathway. J. Neurosci. 6: 3492-3498, 1986.
46. RODRIGUEZ, R. AND HABERLY, L. B. Analysis of synaptic events in the opossum piriform cortex with improved current source-density techniques. J. Neurophysiol. 61: 702-718, 1989.
47. SCHARFMAN, H. E. Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J. Neurosci. 11: 1680-1673, 1991.
48. SCHARFMAN, H. E., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37: 693-707, 1990.
49. SCHARFMAN, H. E. AND SCHWARTZKROIN, P. A. Electrophysiology of morphologically identified mossy cells of the rat dentate hilus. J. Neurosci. 8: 3412-3421, 1988.
50. SCHLESSINGER, A. R., COWAN, W. M., AND GOTTLIEB, D. L An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J. Comp. Neurol. 159: 149-176, 1975.
51. SERESS, L. AND POKORNY, J. Structure of the granule cell layer of the rat dentate gyrus: a light microscopic and Golgi study. J. Anat. 133: 181-195, 1981.
52. SERESS, L. AND RIBAK, C. E. GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp. Brain Res. 50: 173-182, 1983.
53. SERESS, L. AND RIBAK, C. E. Direct commissural connections to the basket cells of the hippocampal dentate gyrus: anatomical evidence for feedforward inhibition. J. Neurocytol. 13: 215-225, 1984.
54. SLOVITER, R. S. Feedforward and feedback inhibition of hippocampal principle cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus 1: 31-40, 1991.
55. SOLTESZ, I. AND JONES, R. G. The direct perforant path input to CA1: excitatory or inhibitory? Hippocampus 5: 101-103, 1995.
56. SPERTI, T., GESSI, F., SANSEVERINO, V., AND SANSEVERINO, E. R. Synaptic organization of commissural projections of the hippocampal region in the guinea pig. I. Dorsal psalterium. mode of activation of granule cells and CA1 pyramidal neurons. Arch. Sci. Biol. 54: 141-182, 1970.
57. STEWARD, O., WHTTE, W. F., COTMAN, C. W., AND LYNCH, G. Potentiation of excitatory synaptic transmission in the normal and in the reinnervated dentate gyrus of the rat. Exp. Brain Res. 26: 423-441, 1976.
58. SWANSON, L. W., WYSS, J. M., AND COWAN, W. M. An autoradiographic study of the organization of intrahippocampal association pathways. J. Comp Neurol. 181: 681-716, 1978.
59. THALMAN, R. AND AYALA, G. A late increase in potassium conductance follows synaptic stimulation of granule neurons in the dentate gyms. Neurosci. Lett. 29: 243-248, 1982.
60. TREVES, A. AND ROLLS, E. T. Computational analysis of the role of the hippocampus in memory. Hippocampus 4: 374-391, 1994.
61. WHITE, G., LEVY, W. B., AND STEWARD, O. Spatial overlap between populations of synapses determines the extent of their associative interaction during the induction of long-term potentiation and depression. J. Neurophysiol. 64: 1186-1198, 1990.
62. WHITE, W. F., GOLDOWITZ, D., LYNCH, G., AND COTMAN, C. W. Electrophysiological analysis of the projection from the contralateral entorhinal cortex to the dentate gyrus in normal rats. Brain Res. 114: 201-209, 1976.
63. WILSON, R. C., LEVY, W. B., AND STEWARD, O. Functional effects of lesion-induced plasticity, long-term potentiation in normal and lesion-induced temporodentate connections. Brain Res. 176: 65-78, 1979.
64. YECKEL, M. F. AND BERGER, T. W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. Natl. Acad. Sci. USA 87: 5832-5836, 1990.
65. ZIMMER, J Ipsilateral afferents to the commissural zone of the fascia dentata, demonstrated in decommissurated rats by silver impregnation. J. Comp. Neurol. 142: 393-416, 1971