Defined types of cortical interneurone structure space and spike timing in the hippocampus

Journal of Physiology

Volumn 562, Issue 1, 2005, Pages 9-26

  Somogyi, Peter ^a   Klausberger, Thomas ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; MEMBRANE PROTEIN; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; CALBINDIN; CALRETININ; CHOLECYSTOKININ; METABOTROPIC GLUTAMATE RECEPTOR 1ALPHA; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 7; METABOTROPIC RECEPTOR 8; MUSCARINIC M2 RECEPTOR; NUCLEAR FACTOR Y; PARVALBUMIN; SOMATOSTATIN; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VESICULAR GLUTAMATE TRANSPORTER 3;

ANIMAL BEHAVIOR; BRAIN CORTEX; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE; CELL POPULATION; CELL STRUCTURE; CELL SYNCHRONIZATION; CELL TYPE; CELLULAR DISTRIBUTION; ELECTROENCEPHALOGRAM; GABAERGIC TRANSMISSION; HIPPOCAMPUS; INNERVATION; INTERNEURON; NERVE CELL NETWORK; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; SPIKE WAVE; SYNAPSE; ACTION POTENTIAL; ARTICLE; BRAIN CELL; DENDRITE; FIRING RATE; GABAERGIC SYSTEM; GAMMA RHYTHM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MEMBRANE POTENTIAL; NERVE PROJECTION; NONHUMAN; PERFORANT NERVE TRACT; SCHAFFER COLLATERAL PATHWAY; STRATUM LACUNOSUM MOLECULARE; STRATUM RADIATUM; THETA RHYTHM;

ANIMALS; BRAIN; CEREBRAL CORTEX; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMANS; INTERNEURONS; NEURONS; THETA RHYTHM;

EID: 13444254358     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.078915     Document Type: Review

References (112)

1. Acsady L, Arabadzisz D & Freund TF (1996a). Correlated morphological and neurochemical features identify different subsets of vasoactive intestinal polypeptide-immunoreactive interneurons in rat hippocampus. Neuroscience 73, 299-315.
2. Acsady L, Gorcs TJ & Freund TF (1996b). Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73, 317-334.
3. Ali AB, Bannister AP & Thomson AM (1999). IPSPs elicited in CA1 pyramidal cells by putative basket cells in slices of adult rat hippocampus. Eur J Neurosci 11, 1741-1753.
4. Amaral DG & Witter MP (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-591.
5. Andersen P, Eccles JC & Loyning Y (1963). Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 198, 540-542.
6. Aradi I, Santhakumar V, Chen K & Soltesz I (2002). Postsynaptic effects of GABAergic synaptic diversity: regulation of neuronal excitability by changes in IPSC variance. Neuropharm 43 511-522.
7. Baimbridge KG & Miller JJ (1982). Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245, 223-229.
8. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger H et al. (2002). Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Nat Acad Sci U S A 99, 13222-13227.
9. Baude A, Nusser Z, Roberts JDB, Mulvihill E, McIlhinney RAJ & Somogyi P (1993). The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771-787.
10. Berger H (1929). Ueber das Elektroenkephalogram des Menschen. Erste Mitteilung Arch Psychiat Nervenkr 87, 529-570.
11. Blasco-Ibanez JM & Freund TF (1995). Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7, 2170-2180.
12. Buhl EH, Cobb SR, Halasy K & Somogyi P (1995). Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7, 1989-2004.
13. Buhl EH, Halasy K & Somogyi P (1994a). Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368, 823-828.
14. Buhl EH, Han Z-S, Lorinczi Z, Stezhka VV, Karnup SV & Somogyi P (1994b). Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J Neurophysiol 71, 1289-1307.
15. Buhl EH, Szilagyi T, Halasy K & Somogyi P (1996). Physiological properties of anatomically identified basket and bistratified cells in the CA1 area of the rat hippocampus in vitro. Hippocampus 6, 294-305.
16. Buzsaki G (1989). Two-stage model of memory trace formation: a role of 'noisy' brain states. Neuroscience 31, 551-570.
17. Buzsaki G (2002). Theta oscillations in the hippocampus. Neuron 33, 325-340.
18. Buzsaki G & Draguhn A (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929.
19. Buzsaki G, Leung L-W & Vanderwolf CH (1983). Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev 6, 139-171.
20. Cobb SR, Buhl EH, Halasy K, Paulsen O & Somogyi P (1995). Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78.
21. Cobb SR, Halasy K, Vida I, Nyiri G, Tamas G, Buhl EH et al. (1997). Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus. Neuroscience 79, 629-648.
22. Cope DW, Maccaferri G, Márton LF, Roberts JDB, Cobden PM & Somogyi P (2002). Cholecystokinin-immunopositive basket and Schaffer collateral-associated interneurones target different domains of pyramidal cells in the CA1 area of the rat hippocampus. Neuroscience 109 63-80.
23. Cossart R, Esclapez M, Hirsch JC, Bernard C & Ben-Ari Y (1998). GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1, 470-478.
24. Csicsvari J, Hirase H, Czurko A, Mamiya A & Buzsaki G (1999). Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19, 274-287.
25. Csicsvari J, Hirase H, Mamiya A & Buzsaki G (2000). Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585-594.
26. Csicsvari J, Jamieson B, Wise KD & Buzsaki G (2003). Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37, 311-322.
27. Dalezios Y, Lujan R, Shigemoto R, Roberts JDB & Somogyi P (2002). Enrichment of mGluR7a in the presynaptic active zones of GABAergic and non-GABAergic terminals on interneurons in the rat somatosensory cortex. Cereb Cortex 12, 961-974.
28. Deuchars J & Thomson AM (1996). CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74, 1009-1018.
29. Dolleman-van der Weel MJ & Witter MP (1996). Projections from the nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculum in the rat arise from different populations of neurons. J Comp Neurol 364, 637-650.
30. Ferraguti F, Cobden P, Pollard M, Cope D, Shigemoto R, Watanabe M et al. (2004). Immunolocalization of metabotropic glutamate receptor 1a (mGluR1a) in distinct classes of interneuron in the CA1 region of the rat hippocampus. Hippocampus 14, 193-215.
31. Földy C, Aradi I, Howard A & Soltesz I (2003). Diversity beyond variance: modulation of firing rates and network coherence by GABAergic subpopulations. Eur J Neurosci 19, 119-130.
32. Freund TF & Buzsaki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
33. Fukuda T & Kosaka T (2000). Gap junctions linking dendritic network gabaergic interneurons hippocampus. J Neurosci 20, 1519-1528.
34. Ganter P, Szücs P, Paulsen O & Somogyi P (2004). Properties of horizontal axo-axonic cells in stratum oriens of the hippocampal CA1 area of rats in vitro. Hippocampus 14, 232-243.
35. A receptors containing the α 1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons. Eur J Neurosci 6 837-853.
36. Gillies MJ, Traub RD, LeBeau FE, Davies CH, Gloveli T, Buhl EH et al. (2002) A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol 543, 779-793.
37. Golding NL & Spruston N (1998). Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21, 1189-1200.
38. Grastyan E, Lissak K, Madarasz I & Donhoffer H (1959). Hippocampal electrical activity during the development of conditioned reflexes. Electroencephalogr Clin Neurophysiolsupplement 11, 409-430.
39. Gulyas AI, Hajos N & Freund TF (1996). Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16, 3397-3411.
40. Gulyas AL, Hajos N, Katona I & Freund TF (2003). Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum. Eur J Neurosci 17, 1861-1872.
41. Gulyas AI, Toth K, McBain CJ & Freund TF (1998). Stratum radiatum giant cells: a type of principal cell in the rat hippocampus. Eur J Neurosci 10, 3813-3822.
42. Hájos N & Mody I (1997). Synaptic communication among hippocampal interneurons: Properties of spontaneous IPSCs in morphologically identified cells. J Neurosci 17, 8427-8442.
43. Hájos N, Papp EC, Acsady L, Levey AL & Freund TF (1998). Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82, 355-376.
44. Halasy K, Buhl EH, Lorinczi Z, Tamas G & Somogyi P (1996). Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6, 306-329.
45. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragol G, Czurkó A et al. (2002). Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738-741.
46. Harris KM, Marshall PE & Landis DMD (1985). Ultrastructural study of cholecystokinin-immunoreactive cells and processes in area CA1 of the rat hippocampus. J Comp Neurol 233, 147-158.
47. Ishizuka N, Weber J & Amaral DG (1990). Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295, 580-623.
48. Jarosiewicz B, McNaughton BL & Skaggs WE (2002). Hippocampal population activity during the small-amplitude irregular activity state in the rat. J Neurosci 22, 1373-1384.
49. Jinno S & Kosaka T (2002). Immunocytochemical characterization of hippocamposeptal projecting GABAergic nonprincipal neurons in the mouse brain: a retrograde labeling study. Brain Res 945, 219-231.
50. Kamondi A, Acsady L, Wang X-J & Buzsaki G (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity-dependent phase-precession of action potentials. Hippocampus 8, 244-261.
51. Katona I, Acsady L & Freund TF (1999a). Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88, 37-55.
52. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K et al. (1999b). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19, 4544-4558.
53. Katsumaru H, Kosaka T, Heizmann CW & Hama K (1988). Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 72, 363-370.
54. Kawaguchi Y & Kubota Y (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cerebral Cortex 7, 476-486.
55. B receptors. J Neurophysiol 74, 2126-2137.
56. Klausberger T, Magill PJ, Marton L, Roberts JDB, Cobden PM, Buzsdki G et al. (2003). Brain state- and cell type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848.
57. Klausberger T, Marton LF, Baude A, Roberts JDB, Magill P & Somogyi P (2004). Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7 41-47.
58. A receptors in the hippocampus. J Neurosci 22, 2513-2521.
59. Konopacki J, Bland BH, Maclver MB & Roth SH (1987). Cholinergic theta rhythm in transected hippocampal slices: independent CA1 and dentate generators. Brain Res 436, 217-222.
60. Li X-G, Somogyi P, Tepper JM & Buzsaki G (1992). Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus. Exp Brain Res 90, 519-525.
61. Li XG, Somogyi P, Ylinen A & Buzsaki G (1994). The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339, 181-208.
62. Lorente de No R (1934). Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46, 113-177.
63. Maccaferri G & McBain CJ (1996). Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16, 5334-5343.
64. Maccaferri G, Roberts JDB, Szucs P, Cottingham CA & Somogyi P (2000). Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol 524, 91-116.
65. Magee JC & Johnston D (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213.
66. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G & Wu C (2004). Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5, 793-807.
67. McBain CJ, DiChiara TJ & Kauer JA (1994). Activation of metabotropic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14, 4433-4445.
68. Morales M & Bloom FE (1997). The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17, 3157-3167.
69. Morales M, Wang SD, DiazRuiz O & Jho DHJ (2004). Cannabinoid CB1 receptor and serotonin 3 receptor subunit A (5-HT3A) are co-expressed in GABA neurons in the rat telencephalon. J Comp Neurol 468, 205-216.
70. Nunzi MG, Gorio A, Milan F, Freund TF, Somogyi P & Smith AD (1985). Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and non-pyramidal neurons in the hippocampus. J Comp Neurol 237, 485-505.
71. A receptor in relation to specific GABAergic synapses in the dentate gyrus. Eur J Neurosci 7, 630-646.
72. A receptor is concentrated in both inhibitory and excitatory synapses on cerebellar granule cells. J Neurosci 16 103-114.
73. A receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13, 428-442.
74. O'Keefe J (1976). Place units in the hippocampus of the freely moving rat. Exp Neurol 51, 78-109.
75. O'Keefe J & Recce ML (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3 317-330.
76. Oliva AA, Jiang M, Lam T, Smith KL & Swann JW (2000). Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20, 3354-3368.
77. Parra P, Gulyas AI & Miles R (1998). How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983-993.
78. 2+ : dual recordings in slices of adult rat hippocampus. Eur J Neurosci 11, 3552-3564.
79. Pawelzik H, Hughes DI & Thomson AM (2002). Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 443, 346-367.
80. A receptor ligands. J Physiol 546, 701-716.
81. Penttonen M, Nurminen N, Miettinen R, Sirvio J, Henze DA, Csicsvari J et al. (1999). Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges in Wistar rats. Neuroscience 94, 735-743.
82. Pikkarainen M, Ronkko S, Savander V, Insausti R & Pitkanen A (1999). Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol 403, 229-260.
83. Ramon y Cajal S (1893). Estructura del asta de ammon y fascia dentata. Anal Soc Espan Historia Natural 22, 53-114.
84. Ranck JB (1973). Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. Part 1. Behavioral correlates and firing repertoires. Exp Neurol 42, 461-531.
85. Ribak CE (1978). Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase. J Neurocytol 7, 461-478.
86. Rockland KS & Ichinohe N (2004). Some thoughts on cortical minicolumns. Exp Brain Res 158, 265-277.
87. Shigemoto R, Kulik A, Roberts JDB, Ohishi H, Nusser Z, Kaneko T et al. (1996a). Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381, 523-525.
88. Sik A, Penttonen M, Ylinen A & Buzsaki G (1995). Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15, 6651-6665.
89. Sik A, Ylinen A, Penttonen M & Buzsaki G (1994). Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265 1722-1724.
90. Singer W (1999). Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49-65.
91. Skaggs WE, McNaughton BL, Wilson MA & Barnes CA (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172.
92. Soltesz I & Deschenes M (1993). Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70, 97-116.
93. Somogyi J, Baude A, Omori Y, Shimizu H, El Mestikawy S, Fukaya M et al. (2004). GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur J Neurosci 19, 552-569.
94. Somogyi P, Dalezios Y, Luján R, Roberts JDB, Watanabe M & Shigemoto R (2003). High level of mGluR7 in the presynaptic active zones of select populations of GABAergic terminals innervating interneurones in the rat hippocampus. Eur J Neurosci 17, 2503-2520.
95. A receptor is concentrated in synaptic junctions containing the α1 and β2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology 35, 1425-1444.
96. Somogyi P, Nunzi MG, Gorio A & Smith AD (1983). A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res 259, 137-142.
97. Somogyi P, Tamas G, Lujan R & Buhl EH (1998). Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26, 113-135.
98. Steriade M (1997). Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cerebral Cortex 7, 583-604.
99. Steriade M (2001). Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86, 1-39.
100. Steriade M & Timofeev I (2003). Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37, 563-576.
101. Szentagothai J (1975). The 'module-concept' in cerebral cortex architecture. Brain Res 95, 475-496.
102. Tamás G, Lörincz A, Simon A & Szabadics S (2003). Identified sources and targets of slow inhibition in the neocortex. Science 299, 1902-1905.
103. Thomson AM, Bannister AP, Hughes DI & Pawelzik H (2000). Differential sensitivity to Zolpidem of IPSPs activated by morphologically identified CA1 interneurons in slices of rat hippocampus. Eur J Neurosci 12, 425-436.
104. Thomson AM, West DC, Wang Y & Bannister AP (2002). Synaptic connections and small circuits involving excitatory and inhibitory neurons in layer 2-5 of adult rat and cat neocortex: Triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12, 936-953.
105. Toth K, Borhegyi Z & Freund TF (1993). Postsynaptic targets of GABAergic hippocampal neurons in the medial septum diagonal band of broca complex. J Neurosci 13, 3712-3724.
106. Toth K, Freund TF & Miles R (1997). Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol 500, 463-474.
107. Traub RD, Draguhn A, Whittington MA, Baldeweg T, Bibbig A, Buhl EH et al. (2002). Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Rev Neurosci 13, 1-30.
108. Tsou K, Mackie K, Sanudo-Pena MC & Walker JM (1999). Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 9, 969-975.
109. Van Groen T & Wyss JM (1990). Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 302 515-528.
110. Vanderwolf CH (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26, 407-418.
111. Vida I, Halasy K, Szinyei C, Somogyi P & Buhl EH (1998). Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506, 755-773.
112. Zappone CA & Sloviter RS (2001). Commissurally projecting inhibitory interneurons of the rat hippocampal dentate gyrus: a colocalization study of neuronal markers and the retrograde tracer Fluoro-Gold. J Comp Neurol 441, 324-344.