Perirhinal cortex input to the hippocampus in the rat: Evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study

European Journal of Neuroscience

Volumn 11, Issue 11, 1999, Pages 4119-4133

  Naber, P A ^a   Witter, M P ^a   Lopes Da Silva, F H ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Anterograde and retrograde tracers; Area CA1; Dentate gyrus; In vivo electrophysiology; Lateral entorhinal cortex; Learning and memory; Subiculum

Indexed keywords

TRACER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; DENTATE GYRUS; ELECTRIC POTENTIAL; ELECTROSTIMULATION; FEMALE; HIPPOCAMPUS; LATENT PERIOD; MEMORY; NERVE TRACT; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RAT; STRUCTURE ACTIVITY RELATION; SUBICULUM; SYNAPTIC TRANSMISSION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; AXONAL TRANSPORT; BIOTIN; CEREBRAL CORTEX; DEXTRANS; ELECTROPHYSIOLOGY; EVOKED POTENTIALS; FEMALE; FLUORESCENT DYES; HIPPOCAMPUS; NEURAL PATHWAYS; PHYTOHEMAGGLUTININS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 0032727231     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00835.x     Document Type: Article

References (44)

1. Amaral, D.G. & Witter, M.P. (1995) The hippocampal formation. In Paxinos, G. (ed.), The Rat Nervous System, 2nd ed. Academic Press, London, pp. 443-493.
2. Burwell, R.D. & Amaral, D.G. (1998) Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J. Comp. Neurol., 391, 293-321.
3. Burwell, R.D., Witter, M.P. & Amaral, D.G. (1995) Perirhinal and postrhinal cortices of the rat: a review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus, 5, 390-408.
4. Canning, K.J. & Leung, L.S. (1997) Lateral-entorhinal, perirhinal and amygdala-entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: a current source density study. Hippocampus, 7, 643-655.
5. Cohen, N.J. & Eichenbaum, H. (1993) Memory, Amnesia, and the Hippocampal System. The MIT Press, Cambridge, MA, USA.
6. Dolleman-Van der Weel, M.J., Wouterlood, F.G. & Witter, M.P. (1994) Multiple anterograde tracing, combining Phaseolus vulgaris leucoagglutinin with rhodamine- and biotin-conjugated dextran amine. J. Neurosci. Meth., 51, 9-21.
7. Dolleman-Van der Weel, M.J., Lopes da Silva, F.H. & Witter, M.P. (1997) Nucleus reuniens thalami modulates activity in hippocampal field CA1 through excitatory and inhibitory mechanisms. J. Neurosci., 17, 5640-5650.
8. Dolorfo, C.L. & Amaral, D.G. (1998) Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol., 398, 25-48.
9. Eichenbaum, H., Otto, T. & Cohen, N.J. (1994) Two functional components of the hippocampal memory system. Brain Behav. Sci., 17, 449-518.
10. Freeman, J.A. & Nicholson, C. (1975) Experimental optimization of current source-density technique for Anuran cerebellum. J. Neurophysiol., 38, 369-382.
11. Gray, J.A. (1982) The Neuropsychology of Anxiety (Oxford Psychology Series). Oxford University Press, Oxford.
12. Insausti, R., Herrero, M.T. & Witter, M.P. (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus, 7, 146-183.
13. Köhler, C. (1988) Intrinsic projections of the retrohippocampal region in the rat brain. III. The lateral entorhinal area. J. Comp. Neurol., 271, 208-228.
14. Kosel, K.C., van Hoesen, G.W. & Rosene, D.L. (1983) A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat. Brain Res., 269, 347-351.
15. Leonard, B.W., Amaral, D.G., Squire, L.R. & Zola-Morgan, S. (1995) Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex. J. Neurosci., 15, 5637-5659.
16. Leung, L.S. (1979) Potentials evoked by alvear tract in hippocampal CA1 region of rats. II Spatial field analysis. J. Neurophysiol., 42, 1571-1589.
17. Leung, L.S., Roth, L. & Canning, K.J. (1995) Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. J. Neurophysiol., 73, 2392-2403.
18. Liu, P. & Bilkey, D.K. (1996) Direct connections between perirhinal cortex and hippocampus is a major constituent of the lateral perforant path. Hippocampus, 6, 125-134.
19. Liu, P. & Bilkey, D.K. (1997) Current source density analysis of the potential evoked in hippocampus by perirhinal cortex stimulation. Hippocampus, 7, 389-396.
20. Lopes da Silva, F.H. (1996) The generation of electric and magnetic signals of the brain by local networks. In Greger, R. & Windhorst, U. (eds), Comprehensive Human Physiology, Vol. 1. Springer, Berlin Heidelberg, pp. 509-531.
21. Lopes da Silva, F.H., Witter, M.P., Boeijinga, P.H. & Lohman, A.H.M. (1990) Anatomical organization and physiology of the limbic system. Physiol. Rev., 70, 453-511.
22. McClelland, J.L. & Goddard, N.H. (1996) Considerations arising from a complementary learning systems perspective of hippocampus and neocortex. Hippocampus, 6, 654-665.
23. McIntyre, D.C., Kelly, M.E. & Staines, W.A. (1996) Efferent projections of the anterior perirhinal cortex in the rat. J. Comp. Neurol., 369, 302-318.
24. McNaughton, B.L. (1980) Evidence for two physiologically distinct perforant pathways to the fascia dentate. Brain Res., 199, 1-19.
25. Meunier, M., Hadfield, W., Bachevalier, J. & Murray, E.A. (1996) Effects of rhinal cortex lesions combined with hippocampectomy on visual recognition memory in rhesus monkeys. J. Neurophysiol., 75, 1190-1205.
26. Murray, E.A. (1996) What have ablation studies told us about the neural substrates of stimulus memory? Semin. Neurosci., 8, 13-22.
27. Naber, P.A. & Witter, M.P. (1998) Subicular efferents are organized mostly as parallel projections: a double-labeling, retrograde-tracing study in the rat. J. Comp. Neurol., 393, 284-297.
28. Naber, P.A., Caballero-Bleda, M., Jorritsma-Byham, B. & Witter, M.P. (1997) Parallel input to the hippocampal memory system through peri- and postrhinal cortices. Neuroreport, 8, 2617-2621.
29. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, San Diego, CA.
30. Ruth, R.E., Collier, T.J. & Routtenberg, A. (1988) Topographical relationship between the entorhinal cortex and the dentate septotemporal axis in rats: II. Cells projecting from lateral entorhinal subdivisions. J. Comp. Neurol., 270, 153-184.
31. Squire, L.R. & Alvarez, P. (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr. Opin. Neurobiol., 5, 169-177.
32. Squire, L.R. & Zola, S.M. (1997) Amnesia, memory and brain systems. Phil. Trans. R. Soc. Lond. B, 352, 1663-1673.
33. Steward, O. (1976) Topographic organization of the projections from the entorhinal area to the hippocampal formation in the rat. J. Comp. Neurol., 167, 285-314.
34. Suzuki, W.A. & Amaral, D.G. (1994) Topographic organization of the reciprocal connections between the monkey entorhinal and the perirhinal and parahippocampal cortices. J. Neurosci., 14, 1856-1877.
35. Suzuki, W.A., Zola-Morgan, S., Squire, L.R. & Amaral, D.G. (1993) Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting impairment in the visual and tactual modalities. J. Neurosci., 13, 2430-2451.
36. Tamamaki, N. & Nojyo, Y. (1995) Preservation of topography in the connections between the subiculum, field CA1 and the entorhinal cortex in rats. J. Comp. Neurol., 353, 379-390.
37. Tulving, E. & Markowitsch, H.J. (1997) Memory beyond the hippocampus. Curr. Opin. Neurobiol., 7, 209-216.
38. Van Groen, T. & Lopes da Silva, F.H. (1985) Septotemporal distribution of entorhinal projections to the hippocampus in the cat, electrophysiological evidence. J. Comp. Neurol., 238, 1-9.
39. Witter, M.P. (1993) Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus, 3, 33-44.
40. Witter, M.P. & Groenewegen, H.J. (1992) Organizational principles of hippocampal connections. In Trimble, M.R. & Bolwig, T.G. (eds), The Temporal Lobes and the Limbic System. Wrightson Biomedical Publishing, Petersfield, pp. 37-60.
41. Witter, M.P., Groenewegen, H.J., Lopes da Silva, F.H. & Lohman, A.H.M. (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol., 33, 161-254.
42. Wyss, J.M. (1981) An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J. Comp. Neurol., 199, 495-512.
43. Zola-Morgan, S., Squire, L.R., Clower, R.P. & Rempel, N.L. (1993) Damage to the perirhinal cortex exacerbates memory impairments following lesions to the hippocampal formation. J. Neurosci., 13, 251-265.
44. Zola-Morgan, S., Squire, L.R. & Ramus, S.J. (1994) Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system. Hippocampus, 4, 483-495.