Cellular neuroanatomy of rat presubiculum

European Journal of Neuroscience

Volumn 37, Issue 4, 2013, Pages 583-597

  Simonnet, Jean ^a   Eugène, Emmanuel ^a   Cohen, Ivan ^a   Miles, Richard ^a   Fricker, Desdemona ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Adaptation; Excitability; Head direction; Morphology; Postsubiculum

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL STRUCTURE; CELL TYPE; CLUSTER ANALYSIS; CONTROLLED STUDY; CYTOLOGY; DENDRITIC CELL; ETORHINAL CORTEX; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE STEADY POTENTIAL; NERVE CELL; NEUROANATOMY; NONHUMAN; PERIARCHICORTEX; PRESUBICULAR CORTEX; PRESUBICULUM; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SOMATIC CELL;

ANIMALS; BRAIN; CLUSTER ANALYSIS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84873996354     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12065     Document Type: Article

References (62)

1. Andjelic, S., Gallopin, T., Cauli, B., Hill, E.L., Roux, L., Badr, S., Hu, E., Tamas, G. & Lambolez, B. (2009) Glutamatergic nonpyramidal neurons from neocortical layer VI and their comparison with pyramidal and spiny stellate neurons. J. Neurophysiol., 101, 641-654.
2. Belgard, T.G., Marques, A.C., Oliver, P.L., Abaan, H.O., Sirey, T.M., Hoerder-Suabedissen, A., García-Moreno, F., Molnár, Z., Margulies, E.H. & Ponting, C.P. (2011) A transcriptomic atlas of mouse neocortical layers. Neuron, 71, 605-616.
3. Boccara, C.N., Sargolini, F., Thoresen, V.H., Solstad, T., Witter, M.P., Moser, E.I. & Moser, M.-B. (2010) Grid cells in pre- and parasubiculum. Nat. Neurosci., 13, 987-994.
4. Burgalossi, A., Herfst, L., von Heimendahl, M., Förste, H., Haskic, K., Schmidt, M. & Brecht, M. (2011) Microcircuits of functionally identified neurons in the rat medial entorhinal cortex. Neuron, 70, 773-786.
5. Cacucci, F., Lever, C., Wills, T.J., Burgess, N. & O'keefe, J. (2004) Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J. Neurosci., 24, 8265-8277.
6. Canto, C.B. & Witter, M.P. (2012) Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus, 22, 1277-1299.
7. Canto, C.B., Wouterlood, F.G. & Witter, M.P. (2008) What does the anatomical organization of the entorhinal cortex tell us? Neural Plast., 2008, 1-18.
8. Cauli, B., Porter, J.T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B. & Audinat, E. (2000) Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc. Natl. Acad. Sci. USA, 97, 6144-6149.
9. Chrobak, J.J. & Buzsaki, G. (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci., 16, 3056-3066.
10. Cohen, I. & Miles, R. (2000) Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus. J. Physiol. (Lond.), 524 Pt 2, 485-502.
11. Connors, B.W. & Gutnick, M.J. (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci., 13, 99-104.
12. Connors, B.W., Gutnick, M.J. & Prince, D.A. (1982) Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol., 48, 1302-1320.
13. Ding, S.L. & Rockland, K.S. (2001) Modular organization of the monkey presubiculum. Exp. Brain Res., 139, 255-265.
14. Douglas, R.J. & Martin, K.A.C. (2007) Mapping the matrix: the ways of neocortex. Neuron, 56, 226-238.
15. Epsztein, J., Brecht, M. & Lee, A.K. (2011) Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron, 70, 109-120.
16. Filimonoff, I.N. (1947) A rational subdivision of the cerebral cortex. Arch. Neurol. Psychiatry, 58, 296-311.
17. Fino, E. & Yuste, R. (2011) Dense inhibitory connectivity in neocortex. Neuron, 69, 1188-1203.
18. + current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices. J. Physiol. (Lond.), 493, 83-97.
19. Fricker, D., Verheugen, J.A. & Miles, R. (1999) Cell-attached measurements of the firing threshold of rat hippocampal neurones. J. Physiol. (Lond.), 517, 791-804.
20. + current. J. Physiol. (Lond.), 587, 4249-4264.
21. Funahashi, M. & Stewart, M. (1997a) Presubicular and parasubicular cortical neurons of the rat: functional separation of deep and superficial neurons in vitro. J. Physiol. (Lond.), 501, 387-403.
22. Funahashi, M. & Stewart, M. (1997b) Presubicular and parasubicular cortical neurons of the rat: electrophysiological and morphological properties. Hippocampus, 7, 117-129.
23. Gasparini, S., Migliore, M. & Magee, J.C. (2004) On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci., 24, 11046-11056.
24. Goldman-Rakic, P.S., Selemon, L.D. & Schwartz, M.L. (1984) Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience, 12, 719-743.
25. van Groen, T. & Wyss, J.M. (1990) The connections of presubiculum and parasubiculum in the rat. Brain Res., 518, 227-243.
26. Hamam, B.N., Kennedy, T.E., Alonso, A. & Amaral, D.G. (2000) Morphological and electrophysiological characteristics of layer V neurons of the rat medial entorhinal cortex. J. Comp. Neurol., 418, 457-472.
27. Honda, Y., Umitsu, Y. & Ishizuka, N. (2008) Organization of connectivity of the rat presubiculum: II. Associational and commissural connections. J. Comp. Neurol., 506, 640-658.
28. Honda, Y., Furuta, T., Kaneko, T., Shibata, H. & Sasaki, H. (2011) Patterns of axonal collateralization of single layer V cortical projection neurons in the rat presubiculum. J. Comp. Neurol., 519, 1395-1412.
29. Isaacson, J.S. & Scanziani, M. (2011) How inhibition shapes cortical activity. Neuron, 72, 231-243.
30. Jarsky, T., Mady, R., Kennedy, B. & Spruston, N. (2008) Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus. J. Comp. Neurol., 506, 535-547.
31. Jerome, J., Foehring, R.C., Armstrong, W.E., Spain, W.J. & Heck, D.H. (2011) Parallel optical control of spatiotemporal neuronal spike activity using high-speed digital light processing. Front. Syst. Neurosci., 5, 70.
32. Jia, H., Rochefort, N.L., Chen, X. & Konnerth, A. (2010) Dendritic organization of sensory input to cortical neurons in vivo. Nature, 464, 1307-1312.
33. Katzner, S., Busse, L. & Carandini, M. (2011) GABAA inhibition controls response gain in visual cortex. J. Neurosci., 31, 5931-5941.
34. Kononenko, N.L. & Witter, M.P. (2012) Presubiculum layer III conveys retrosplenial input to the medial entorhinal cortex. Hippocampus, 22, 881-895.
35. Kruger, L., Saporta, S. & Swanson, L.W. (1995) Photographic Atlas of the Rat Brain. Cambridge University Press, New York, USA.
36. Longson, D., Longson, C.M. & Jones, E.G. (1997) Localization of CAM II kinase-alpha, GAD, GluR2 and GABA(A) receptor subunit mRNAs in the human entorhinal cortex. Eur. J. Neurosci., 9, 662-675.
37. Lorente de No, R. (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of ammonic system. J. Psychol. Neurol., 46, 113-177.
38. Losonczy, A., Makara, J.K. & Magee, J.C. (2008) Compartmentalized dendritic plasticity and input feature storage in neurons. Nature, 452, 436-441.
39. Lübke, J. & Feldmeyer, D. (2007) Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct. Funct., 212, 3-17.
40. Madison, D.V. & Nicoll, R.A. (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J. Physiol. (Lond.), 354, 319-331.
41. Mountcastle, V.B. (1997) The columnar organization of the neocortex. Brain, 120, 701-722.
42. Nishikawa, S., Goto, S., Hamasaki, T., Yamada, K. & Ushio, Y. (2002) Involvement of reelin and Cajal-Retzius cells in the developmental formation of vertical columnar structures in the cerebral cortex: evidence from the study of mouse presubicular cortex. Cereb. Cortex, 12, 1024-1030.
43. O'Mara, S.M., Commins, S., Anderson, M. & Gigg, J. (2001) The subiculum: a review of form, physiology and function. Prog. Neurobiol., 64, 129-155.
44. Petilla Interneuron Nomenclature Group, Ascoli, G.A., Alonso-Nanclares, L., Anderson, S.A., Barrionuevo, G., Benavides-Piccione, R., Burkhalter, A., Buzsáki, G., Cauli, B., Defelipe, J., Fairén, A., Feldmeyer, D., Fishell, G., Fregnac, Y., Freund, T.F., Gardner, D., Gardner, E.P., Goldberg, J.H., Helmstaedter, M., Hestrin, S., Karube, F., Kisvárday, Z.F., Lambolez, B., Lewis, D.A., Marin, O., Markram, H., Muñoz, A., Packer, A., Petersen, C.C.H., Rockland, K.S., Rossier, J., Rudy, B., Somogyi, P., Staiger, J.F., Tamas, G., Thomson, A.M., Toledo-Rodriguez, M., Wang, Y., West, D.C. & Yuste, R. (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci., 9, 557-568.
45. Ranck, J.J. (1984) Head direction cells in the deep layer of dorsal presubiculum in freely moving rats. Soc. Neurosci. Abstr., 10, 599.
46. Rolls, E.T. (2006) Neurophysiological and computational analyses of the primate presubiculum, subiculum and related areas. Behav. Brain Res., 174, 289-303.
47. Schubert, D., Staiger, J.F., Cho, N., Kötter, R., Zilles, K. & Luhmann, H.J. (2001) Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J. Neurosci., 21, 3580-3592.
48. Shibata, H. & Honda, Y. (2012) Thalamocortical projections of the anterodorsal thalamic nucleus in the rabbit. J. Comp. Neurol., 520, 2647-2656.
49. Shipley, M.T. & Sorensen, K.E. (1975) On the laminar organization of the anterior thalamus projections to the presubiculum in the guinea pig. Brain Res., 86, 473-477.
50. Tahvildari, B. & Alonso, A. (2005) Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons. J. Comp. Neurol., 491, 123-140.
51. Taube, J.S. (2007) The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci., 30, 181-207.
52. Taube, J.S. & Muller, R.U. (1998) Comparisons of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats. Hippocampus, 8, 87-108.
53. Taube, J.S., Muller, R.U. & Ranck, J.B. (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci., 10, 420-435.
54. Thorndike, R.L. (1953) Who belongs in the family? Psychometrika, 18, 267-276.
55. Van Strien, N.M., Cappaert, N.L.M. & Witter, M.P. (2009) The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci., 10, 272-282.
56. Vogt, B.A. & Miller, M.W. (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J. Comp. Neurol., 216, 192-210.
57. Ward, J.H. Jr. (1963) Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc., 58, 236-244.
58. Williams, S.R. & Stuart, G.J. (1999) Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J. Physiol. (Lond.), 521 Pt 2, 467-482.
59. Witter, M.P., Groenewegen, H.J., Lopes da Silva, F.H. & Lohman, A.H. (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol., 33, 161-253.
60. Yoder, R.M. & Taube, J.S. (2011) Projections to the anterodorsal thalamus and lateral mammillary nuclei arise from different cell populations within the postsubiculum: implications for the control of head direction cells. Hippocampus, 21, 1062-1073.
61. Yoder, R.M., Clark, B.J. & Taube, J.S. (2011) Origins of landmark encoding in the brain. Trends Neurosci., 34, 561-571.
62. Yoshida, M. & Hasselmo, M.E. (2009) Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J. Neurosci., 29, 4945-4952.