Significance of the deep layers of entorhinal cortex for transfer of both perirhinal and amygdala inputs to the hippocampus

Neuroscience Research

Volumn 61, Issue 2, 2008, Pages 172-181

  Koganezawa, Noriko ^a   Taguchi, Ayaka ^a   Tominaga, Takashi ^b   Ohara, Shinya ^a   Tsutsui, Ken Ichiro ^a   Witter, Menno P ^c,d   Iijima, Toshio ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^c NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^d Institute for Clinical and Experimental Neurosciences ICEN   (Netherlands)

Author keywords

Amygdala; Entorhinal cortex; Hippocampus; Optical imaging; Perirhinal cortex; Signal gating

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CELL STIMULATION; CONTROLLED STUDY; DENTATE GYRUS; ELECTROSTIMULATION; ENTORHINAL CORTEX; HIPPOCAMPUS; IMAGING; MALE; MEMBRANE POTENTIAL; NERVE CELL NETWORK; NONHUMAN; OPTICS; PRIORITY JOURNAL; RAT; SENSORY SYSTEM; VOLTAGE CLAMP;

AMYGDALA; ANIMALS; ELECTRIC STIMULATION; ENTORHINAL CORTEX; HIPPOCAMPUS; MALE; NEURAL PATHWAYS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR;

EID: 42749087994     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2008.02.007     Document Type: Article

References (54)

1. Barish M.E., Ichikawa M., Tominaga T., Matsumoto G., and Iijima T. Enhanced fast synaptic transmission and a delayed depolarization induced by transient potassium current blockade in rat hippocampal slice as studied by optical recording. J. Neurosci. 16 (1996) 5672-5687
2. Berretta N., and Jones R.S. A comparison of spontaneous EPSCs in layer II and layer IV-V neurons of the rat entorhinal cortex in vitro. J. Neurophysiol. 76 2 (1996) 1089-1100
3. Burwell R.D. The parahippocampal region: corticocortical connectivity. Ann. N. Y. Acad. Sci. 911 (2000) 25-42
4. Burwell R.D., and Amaral D.G. Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J. Comp. Neurol. 391 (1998) 293-321
5. Burwell R.D., and Witter M.P. Basic anatomy of the parahippocampal region in monkeys and rats. In: Witter M.P., and Wouterlood F.G. (Eds). The Parahippocampal Region, Organisation and Role in Cognitive Functions (2002), Oxford University Press, Oxford 35-59
6. Burwell R.D., Witter M.P., and Amaral D.G. Perirhinal and postrhinal cortices of the rat: a review of neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5 (1995) 390-408
7. Cahill L., Babinsky R., Markowitsch H.J., and McGaugh J.L. The amygdala and emotional memory. Nature 28 (1995) 295-296
8. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., Wu J., and McGaugh J.L. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 8016-8021
9. de Curtis M., and Paré D. The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus. Prog. Neurobiol. 74 (2004) 101-110
10. Deller T., Martínez A., Nitsch R., and Frotscher M. A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. J. Neurosci. 16 (1996) 3322-3333
11. Dolorfo C.L., and Amaral D.G. Entorhinal cortex of the rat: organizations of intrinsic connections. J. Comp. Neurol. 398 (1998) 49-82
12. Dugladze T., Heinemann U., and Gloveli T. Entorhinal cortex projection cells to the hippocampal formation in vitro. Brain Res. 905 (2001) 224-231
13. Eichenbaum H., Yonelinas A.P., and Ranganath C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30 (2007) 123-152
14. Faulkner B., and Brown T.H. Morphology and physiology of neurons in the rat perirhinal-lateral amygdala area. J. Comp. Neurol. 411 (1999) 613-642
15. Gloveli T., Dugladze T., Schmitz D., and Heinemann U. Properties of entorhinal cortex deep layer neurons projecting to the rat dentate gyrus. Eur. J. Neurosci. 13 (2001) 413-420
16. Grinvald A., Lieke E.E., Frostig R.D., and Hildesheim R. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci. 14 (1994) 2545-2568
17. Grinvald A., Manker A., and Segal M. Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J. Physiol. 333 (1982) 269-291
18. Gulyás A.I., and Freund T.F. Pyramidal cell dendrites are the primary targets of calbindin D28k-immunoreactive interneurons in the hippocampus. Hippocampus 6 (1996) 525-534
19. Hamann S.B., Ely T.D., Grafton S.T., and Kilts C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat. Neurosci. 2 (1999) 289-293
20. Hjorth-Simonsen A., and Jeune B. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144 (1972) 215-232
21. Iijima T., Kajiwara R., Ichikawa M., and Witter M.P. Long-lasting neural excitation in the deep layer of perirhinal-cortex is necessary for the propagation of neural activity among the entorhinal-perirhinal-temporal cortices. Soc. Neurosci. Abstr. 20 (1994) 800
22. Iijima T., Witter M.P., Ichikawa M., Tominaga T., Kajiwara R., and Matsumoto G. Entorhinal-hippocampal interactions revealed by real-time imaging. Science 272 (1996) 1176-1179
23. Insausti R., Herrero M.T., and Witter M.P. Entorhinal cortex of the rat cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7 (1997) 146-183
24. Kajiwara R., Takashima I., Mimura Y., Witter M.P., and Iijima T. Amygdala input promotes spread of excitatory neural activity from perirhinal cortex to the entorhinal-hippocampal circuit. J. Neurophysiol. 89 (2003) 2176-2184
25. Krettek J.E., and Price J.L. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J. Comp. Neurol. 171 (1977) 157-191
26. Köhler C. A projection from the deep layers of the entorhinal area to the hippocampal formation in the rat brain. Neurosci. Lett. 56 (1985) 13-19
27. Köhler C. The intrinsic connections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J. Comp. Neurol. 246 (1986) 149-169
28. Lingenhöhl K., and Finch D.M. Morphological characterization of rat entorhinal neurons in vivo: soma-dendritic structure and axonal domains. Exp. Brain Res. 84 (1991) 57-74
29. Miettinen M., Koivisto E., Riekkinen P., and Miettinen R. Coexistence of parvalbumin and GABA in nonpyramidal neurons of the rat entorhinal cortex. Brain Res. 706 (1996) 113-122
30. Moyer Jr. J.R., and Brown T.H. Methods for whole-cell recording from visually preselected neurons of perirhinal cortex in brain slices from young and aging rats. J. Neurosci. Methods 86 (1998) 35-54
31. Murray E.A., and Richmond B.J. Role of perirhinal cortex in object perception, memory, and associations. Curr. Opin. Neurobiol. 11 (2001) 188-193
32. Nishijo H., Uwano T., Tamura R., and Ono T. Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. J. Neurophysiol. 79 (1998) 21-36
33. Ono T., Nishijo H., and Uwano T. Amygdala role in conditioned associative learning. Prog. Neurobiol. 46 (1995) 401-422
34. Otsu Y., Maru E., Ohata H., Takashima I., Kajiwara R., and Iijima T. Optical recording study of granule cell activities in the hippocampal dentate gyrus of kainate-treated rats. J. Neurophysiol. 83 (2000) 2421-2430
35. Paz R., Pelletier J.G., Bauer E.P., and Paré D. Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions. Nat. Neurosci. 9 (2006) 1321-1329
36. Pelletier J.G., Apergis-Schoute J., and Paré D. Interaction between amygdala and neocortical inputs in the perirhinal cortex. J. Neurophysiol. 94 (2005) 1837-1848
37. Pikkarainen M., Rönkkö S., Savander V., Insausti R., and Pitkänen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 403 (1999) 229-260
38. Pinto A., Fuentes C., and Paré D. Feedforward inhibition regulates perirhinal transmission of neocortical inputs to the entorhinal cortex: ultrastructural study in guinea pigs. J. Comp. Neurol. 495 (2006) 722-734
39. Richardson M.P., Strange B.A., and Dolan R.J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat. Neurosci. 7 (2004) 278-285
40. Rosenkranz J.A., and Johnston D. State-dependent modulation of amygdala inputs by dopamine-induced enhancement of sodium currents in layer V entorhinal cortex. J. Neurosci. 27 (2007) 7054-7069
41. Steward O., and Scoville S.A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169 (1976) 347-370
42. Suzuki W., and Eichenbaum H. The Neurophysiology of Memory (2000), New York Academy of Sciences, New York
43. Tamamaki N., and Nojyo Y. Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus 3 (1993) 471-480
44. Tominaga T., Tominaga Y., Yamada H., Matsumoto G., and Ichikawa M. Quantification of optical signals with electrophysiological signals in neural activities of Di-4-ANEPPS stained rat hippocampal slices. J. Neurosci. Methods 15 (2000) 11-23
45. van Haeften T., Baks-te-Bulte L., Goede P., Wouterlood F.G., and Witter M.P. Morphological and numerical analysis of synaptic interactions between neurons in the deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 13 (2003) 943-952
46. von Bohlen und Halbach O., and Albrecht D. Reciprocal connections of the hippocampal area CA1, the lateral nucleus of the amygdala and cortical areas in a combined horizontal slice preparation. Neurosci. Res. 44 (2002) 91-100
47. Witter M.P. Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus 3 (1993) 33-44
48. Witter M.P., and Amaral D.G. The hippocampal formation. In: Paxinos G. (Ed). The Rat Nervous System, 3rd ed. (2004), Academic Press, San Diego 635-704
49. Witter M.P., Griffioen A.W., Jorritsma-Byham B., and Krijnen J.L.M. Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci. Lett. 85 (1988) 193-198
50. Witter M.P., and Wouterlood F.G. The Parahippocampal Region. Organization and Role in Cognitive Functions (2002), Oxford University Press, UK
51. Witter M.P., Wouterlood F.G., Naber P.A., and Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Ann. N Y Acad. Sci. 911 (2000) 1-24
52. Wood S.J., and Jones R.S.G. Characteristics of spontaneous GABAA receptor-mediated IPSCs in rat entorhinal cortical neurones. J. Physiol. 515 (1998) 120
53. Woodhall G.L., Bailey S.J., Thompson S.E., Evans D.I., and Jones R.S. Fundamental differences in spontaneous synaptic inhibition between deep and superficial layers of the rat entorhinal cortex. Hippocampus 15 (2005) 232-245
54. Wouterlood F.G., Van Haeften T., Eijkhoudt M., Baks-Te-Bulte L., Goede P.H., and Witter M.P. Input from the presubiculum to dendrites of layer-V neurons of the medial entorhinal cortex of the rat. Brain Res. 1013 (2004) 1-12