Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity

Progress in Brain Research

Volumn 163, Issue , 2007, Pages

  Houser, Carolyn R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

calretinin; GABA; glutamate decarboxylase (GAD); hilus; interneurons; parvalbumin; somatostatin

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; CALCIUM BINDING PROTEIN; CALRETININ; CHOLECYSTOKININ; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; MOLECULAR LAYER; NEUROPEPTIDE; NEUROPEPTIDE Y; PARVALBUMIN; SOMATOSTATIN;

CELL LABELING; CELL TYPE; CELLULAR DISTRIBUTION; DENDRITE; DENDRITIC CELL; DENTATE GYRUS; GRANULE CELL; HUMAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INNERVATION; INTERNEURON; MORPHOLOGICAL TRAIT; NERVE CELL; NERVE CONDUCTION; NERVE ENDING; NERVE PLEXUS; NEUROCHEMISTRY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; REVIEW; RODENT;

EID: 34548279876     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(07)63013-1     Document Type: Review

References (81)

1. Acsády L., Kamondi A., Sik A., Freund T., and Buzsáki G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18 (1998) 3386-3403
2. Acsády L., Katona I., Martinez-Guijarro F.J., Buzsáki G., and Freund T.F. Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J. Neurosci. 20 (2000) 6907-6919
3. Acsády L., Pascual M., Rocamora N., Soriano E., and Freund T.F. Nerve growth factor but not neurotrophin-3 is synthesized by hippocampal GABAergic neurons that project to the medial septum. Neuroscience 98 (2000) 23-31
4. Alonso A., and Kohler C. Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain. Neurosci. Lett. 31 (1982) 209-214
5. Amaral D.G. A Golgi study of cell types in the hilar region of the hippocampus in the rat. J. Comp. Neurol. 182 (1978) 851-914
6. Babb T.L., Pretorius J.K., Kupfer W.R., and Brown W.J. Distribution of glutamate-decarboxylase-immunoreactive neurons and synapses in the rat and monkey hippocampus: light and electron microscopy. J. Comp. Neurol. 278 (1988) 121-138
7. Bakst I., Avendano C., Morrison J.H., and Amaral D.G. An experimental analysis of the origins of somatostatin-like immunoreactivity in the dentate gyrus of the rat. J. Neurosci. 6 (1986) 1452-1462
8. Blasco-Ibáñez J.M., and Freund T.F. Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7 (1997) 307-320
9. Blasco-Ibánez J.M., Martínez-Guijarro F.J., and Freund T.F. Recurrent mossy fibers preferentially innervate parvalbumin-immunoreactive interneurons in the granule cell layer of the rat dentate gyrus. Neuroreport 11 (2000) 3219-3225
10. Buckmaster P.S., and Dudek F.E. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol. 385 (1997) 385-404
11. Buckmaster P.S., and Jongen-Rêlo A.L. Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J. Neurosci. 19 (1999) 9519-9529
12. Buckmaster P.S., Kunkel D.D., Robbins R.J., and Schwartzkroin P.A. Somatostatin-immunoreactivity in the hippocampus of mouse, rat, guinea pig, and rabbit. Hippocampus 4 (1994) 167-180
13. Buckmaster P.S., and Schwartzkroin P.A. Interneurons and inhibition in the dentate gyrus of the rat in vivo. J. Neurosci. 15 1 (1995) 774-789
14. Commons K.G., and Milner T.A. Cellular and subcellular localization of delta opioid receptor immunoreactivity in the rat dentate gyrus. Brain Res. 738 (1996) 181-195
15. Czeh B., Hajnal A., and Seress L. NADPH-diaphorase positive neurons of the rat hippocampal formation: regional distribution, total number and colocalization with calcium binding proteins. Prague Med. Rep. 106 (2005) 261-274
16. DeFelipe J. Chandelier cells and epilepsy. Brain 122 Pt 10 (1999) 1807-1822
17. Deller T., and Leranth C. Synaptic connections of neuropeptide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus. J. Comp. Neurol. 300 (1990) 433-447
18. Dragoi G., Carpi D., Recce M., Csicsvari J., and Buzsaki G. Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J. Neurosci. 19 (1999) 6191-6199
19. Drake C.T., and Milner T.A. Mu opioid receptors are extensively co-localized with parvalbumin, but not somatostatin, in the dentate gyrus. Neurosci. Lett. 403 (2006) 176-180
20. Erlander M.G., Tillakaratne N.J.K., Feldblum S., Patel N., and Tobin A.J. Two genes encode distinct glutamate decarboxylases. Neuron 7 (1991) 91-100
21. A receptor. Hippocampus 6 (1996) 225-238
22. Esclapez M., and Houser C.R. Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: evidence from co-localization of pre-prosomatostatin and glutamate decarboxylase mRNAs. Neuroscience 64 (1995) 339-355
23. Esclapez M., Tillakaratne N.J.K., Kaufman D.L., Tobin A.J., and Houser C.R. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J. Neurosci. 14 (1994) 1834-1855
24. Freund T.F., and Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336 (1988) 170-173
25. Freund T.F., and Buzsáki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
26. Fujise N., Liu Y., Hori N., and Kosaka T. Distribution of calretinin immunoreactivity in the mouse dentate gyrus: II. Mossy cells, with special reference to their dorsoventral difference in calretinin immunoreactivity. Neuroscience 82 (1998) 181-200
27. A receptors containing the α1 subunit to neurochemically distinct subpopulations of rat hippocampal interneurons. Eur. J. Neurosci. 6 (1994) 837-853
28. A receptor subunit partnership with high sensitivity to ethanol. Nat. Neurosci. 10 (2007) 40-48
29. Gulyás A.I., Hajos N., Katona I., and Freund T.F. Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum. Eur. J. Neurosci. 17 (2003) 1861-1872
30. Gulyás A.I., Buzsáki G., Freund T.F., and Hirase H. Populations of hippocampal inhibitory neurons express different levels of cytochrome c. Eur. J. Neurosci. 23 (2006) 2581-2594
31. Gulyás A.I., Hájos N., and Freund T.F. Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci. 16 10 (1996) 3397-3411
32. Halasy K., and Somogyi P. Distribution of GABAergic synapses and their targets in the dentate gyrus of rat: a quantitative immunoelectron microscopic analysis. J. Hirnforsch 34 (1993) 299-308
33. Halasy K., and Somogyi P. Subdivision in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5 (1993) 411-429
34. Han Z.-S., Buhl E.H., Lorinczi Z., and Somogyi P. A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur. J. Neurosci. 5 (1993) 395-410
35. Houser C.R., and Esclapez M. Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus 5 (1994) 530-545
36. Houser C.R., Esclapez M., and Zhang N. GABA Neurons of the hippocampal formation: localization, vulnerability and plasticity. In: Martin D.L., and Olsen R.W. (Eds). GABA in the Nervous System: The View at Fifty Years (2000), Lippincott Williams & Wilkins, Philadelphia, PA 337-355
37. Jinno S., Aika Y., Fukuda T., and Kosaka T. Quantitative analysis of GABAergic neurons in the mouse hippocampus, with optical disector using confocal laser scanning microscope. Brain Res. 814 1-2 (1998) 55-70
38. Jinno S., and Kosaka T. Immunocytochemical characterization of hippocamposeptal projecting GABAergic nonprincipal neurons in the mouse brain: a retrograde labeling study. Brain Res. 945 (2002) 219-231
39. Jinno S., and Kosaka T. Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J. Comp. Neurol. 449 (2002) 1-25
40. Jinno S., and Kosaka T. Patterns of expression of neuropeptides in GABAergic nonprincipal neurons in the mouse hippocampus: quantitative analysis with optical disector. J. Comp. Neurol. 461 (2003) 333-349
41. Jinno S., and Kosaka T. Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology. Neurosci. Res. 56 (2006) 229-245
42. Johansen F.F., Zimmer J., and Diemer N.H. Early loss of somatostatin neurons in dentate hilus after cerebral ischemia in the rat precedes CA-1 pyramidal cell loss. Acta Neuropathol. (Berl.) 73 (1987) 110-114
43. Katona I., Acsády L., and Freund T. Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88 (1999) 37-55
44. Kaufman D.L., Houser C.R., and Tobin A.J. Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decarboxylase have distinct intraneuronal distributions and cofactor interactions. J. Neurochem. 56 (1991) 720-723
45. Kiss J., Csaki A., Bokor H., Shanabrough M., and Leranth C. The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]D-aspartate autoradiographic and immunohistochemical study. Neuroscience 97 (2000) 657-669
46. Klausberger T., Marton L.F., O'Neill J., Huck J.H., Dalezios Y., Fuentealba P., Suen W.Y., Papp E., Kaneko T., Watanabe M., Csicsvari J., and Somogyi P. Complementary roles of cholecystokinin and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J. Neurosci. 25 (2005) 9782-9793
47. Kohler C., Eriksson L.G., Davies S., and Chan-Palay V. Co-localization of neuropeptide tyrosine and somatostatin immunoreactivity in neurons of individual subfields of the rat hippocampal region. Neurosci. Lett. 78 (1987) 1-6
48. Lauterborn J.C., Tran T.M., Isackson P.J., and Gall C.M. Nerve growth factor mRNA is expressed by GABAergic neurons in rat hippocampus. Neuroreport 5 (1993) 273-276
49. Liu Y., Fujise N., and Kosaka T. Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description. Exp. Brain Res. 108 (1996) 389-403
50. Maccaferri G., and Lacaille J.C. Interneuron diversity series: hippocampal interneuron classifications - making things as simple as possible, not simpler. Trends Neurosci. 26 (2003) 564-571
51. Maglóczky Z., Acsády L., and Freund T. Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4 (1994) 322-334
52. Martin D.L., Martin S.B., Wu S.J., and Espina N. Cofactor interactions and the regulation of glutamate decarboxylase activity. Neurochem. Res. 16 (1991) 243-249
53. Mátyás F., Freund T.F., and Gulyás A.I. Immunocytochemically defined interneuron populations in the hippocampus of mouse strains used in transgenic technology. Hippocampus 14 (2004) 460-481
54. Miles R., Tóth K., Gulyás A.I., Hájos N., and Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996) 815-823
55. Parra P., Gulyas A.I., and Miles R. How many subtypes of inhibitory cells in the hippocampus?. Neuron 20 (1998) 983-993
56. Pascual M., Rocamora N., Acsády L., Freund T.F., and Soriano E. Expression of nerve growth factor and neurotrophin-3 mRNAs in hippocampal interneurons: morphological characterization, levels of expression, and colocalization of nerve growth factor and neurotrophin-3. J. Comp. Neurol. 395 (1998) 73-90
57. A receptor in a mouse model of temporal lobe epilepsy. J. Neurosci. 24 (2004) 8629-8639
58. Pesold C., Impagnatiello F., Pisu M.G., Uzunov D.P., Costa E., Guidotti A., and Caruncho H.J. Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 3221-3226
59. Ribak C.E. Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase. J. Neurocytol. 7 (1978) 461-478
60. Ribak C.E., Nitsch R., and Seress L. Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J. Comp. Neurol. 300 (1990) 449-461
61. Ribak C.E., and Seress L. Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J. Neurocytol. 12 (1983) 577-597
62. Ribak C.E., Vaughn J.E., and Saito K. Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res. 140 (1978) 315-332
63. Scotti A.L., Bollag O., Kalt G., and Nitsch C. Loss of perikaryal parvalbumin immunoreactivity from surviving GABAergic neurons in the CA1 field of epileptic gerbils. Hippocampus 7 (1997) 524-535
64. Sik A., Penttonen M., and Buzsaki G. Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur. J. Neurosci. 9 (1997) 573-588
65. Sloviter R.S. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235 (1987) 73-76
66. Sloviter R.S., and Nilaver G. Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J. Comp. Neurol. 256 (1987) 42-60
67. Sloviter R.S., Sollas A.L., Barbaro N.M., and Laxer K.D. Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J. Comp. Neurol. 308 (1991) 381-396
68. Somogyi P. A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res. 136 (1977) 345-350
69. Somogyi P., and Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 562 (2005) 9-26
70. Soriano E., and Frotscher M. A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res. 503 (1989) 170-174
71. Soriano E., Nitsch R., and Frotscher M. Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochemical studies. J. Comp. Neurol. 293 (1990) 1-25
72. Sperk G., Marksteiner J., Gruber B., Bellmann R., Mahata M., and Ortler M. Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience 50 (1992) 831-846
73. A receptor subunits in the rat hippocampus I: immunocytochemical distribution of 13 subunits. Neuroscience 80 (1997) 987-1000
74. Stumm R.K., Zhou C., Schulz S., and Hollt V. Neuronal types expressing mu- and delta-opioid receptor mRNA in the rat hippocampal formation. J. Comp. Neurol. 469 (2004) 107-118
75. Szentágothai J. Conceptual models of neural organization. Neurosci. Res. Prog. Bull. 12 (1974) 307-510
76. Toth K., and Freund T.F. Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49 (1992) 793-805
77. Valtschanoff J.G., Weinberg R.J., Kharazia V.N., Nakane M., and Schmidt H.H. Neurons in rat hippocampus that synthesize nitric oxide. J. Comp. Neurol. 331 (1993) 111-121
78. Wittner L., Maglóczky Z., Borhegyi Z., Halász P., Tóth S., Eröss L., Szabó Z., and Freund T.F. Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience 108 (2001) 587-600
79. Woodson W., Nitecka L., and Ben-Ari Y. Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study. J. Comp. Neurol. 280 (1989) 254-271
80. Zappone C.A., and Sloviter R.S. 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 (2001) 324-344
81. Zipp F., Nitsch R., Soriano E., and Frotscher M. Entorhinal fibers form synaptic contacts on parvalbumin-immunoreactive neurons in the rat fascia dentata. Brain Res. 495 (1989) 161-166