Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons

Journal of Neuroscience

Volumn 20, Issue 9, 2000, Pages 3354-3368

  Oliva Jr , Anthony A ^a,b   Jiang, Minghui ^a,b   Lam, Trang ^a,b   Smith, Karen L ^a,b   Swann, John W ^a,b  

^a Cain Foundation Laboratories   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cortex; EGFP; GABA; GABAergic neurons; Gad1; GAD67; GFP; Glutamic acid decarboxylase; Green fluorescent protein; Hippocampus; Interneurons; Metabotropic glutamate receptor; MGluR1; MGluR1a; Somatostatin; Transgenic mice

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; FEEDBACK SYSTEM; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; MOLECULAR MODEL; MOUSE; NEOCORTEX; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSGENIC MOUSE;

EID: 0343569849     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-09-03354.2000     Document Type: Article

References (74)

1. Alcántara S,Ruiz M, D'Arcangelo G, Ezan F, de Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779-7799.
2. Alonso A, Köhler C (1982) Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain. Neurosci Lett 31:209-214.
3. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P (1993) The metabotropic glutamate receptor (mG1uR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
4. Bergmann I, Nitsch R, Frotscher M (1991) Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry. Anat Embryol (Berl) 184:403-404.
5. Bissette G (1997) Neuropeptides and Alzheimer's disease pathology. Ann NY Acad Sci 814:17-29.
6. Blasco-Ibáñez 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.
7. 65) suggests that they derive from a common ancestral GAD. Genomics 21:222-228.
8. Busler DE, Li SW (1996) Rapid screening of transgenic type II and type XI collagen knock-out mice with three-primer PCR. Biotechniques 21:1002-1004.
9. Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504-510.
10. 2+ influx. J Neurophysiol 73:2553-2557.
11. Cormack BP, Valdivia RH, Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
12. Dalsgaard CJ, Hokfelt T, Johansson O, Elde R (1981) Somatostatin immunoreactive cell bodies in the dorsal horn and the parasympathetic intermediolateral nucleus of the rat spinal cord. Neurosci Lett 27:335-339.
13. Davies P, Katzman R, Terry RD (1980) Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementia. Nature 288:279-280.
14. Dodt HU, Zieglgänsberger W (1990) Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res 537:333-336.
15. Dodt HU, Zieglgänsberger W (1994) Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci 17:453-458.
16. Esclapez M, Houser CR (1995) Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: evidence from colocalization of pre-prosomatostatin and glutamate decarboxylase messenger RNAs. Neuroscience 64:339-355.
17. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
18. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
19. Göres TJ, Penke B, Böti Z, Katarova Z, Hámori J (1993) Immunohistochemical visualization of a metabotropic glutamate receptor. Neuro-Report 4:283-286.
20. Grouselle D, Winsky-Sommerer R, David JP, Delacourte A, Dournaud P, Epelbaum J (1998) Loss of somatostatin-like immunoreactivity in the frontal cortex of Alzheimer patients carrying the apolipoprotein epsilon 4 allele. Neurosci Lett 255:21-24.
21. Gulyás AI, Miles R, Sík A, Tóth K, Tamamaki N, Freund TF (1993a) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
22. Gulyás AI, Miles R, Hájos N, Freund TF (1993b) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5:1729-1751.
23. Halasy K, Somogyi P (1993) Subdivisions in the multiple GABAergic innervation of granule cells in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:411-429.
24. Hájos N, Mody I (1997) Synaptic communication among hippocampal interneurons: properties of spontaneous IPSCs in morphologically identified cells. J Neurosci 17:8427-8442.
25. Ho RH, Berelowitz M (1984) Somatostatin 28(1-14) immunoreactivity in primary afferent neurons of the rat spinal cord. Neurosci Lett 46:161-166.
26. Hogan B, Beddington R, Costantini F, Lacey E (1994) Manipulating the mouse embryo. Plainview, NY: Cold Spring Harbor Laboratory.
27. Jiang M, Swann JW (1997) Expression of calretinin in diverse neuronal populations during development of rat hippocampus. Neuroscience 81:1137-1154.
28. Johansson O, Hökfelt T, Elde RP (1984) Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13:265-339.
29. Katona I, Acsády L, Gulácsi A, Freund TF (1996) Somatostatin-containing cells in the rat hippocampus: connectivity and heterogeneity. Eur J Neurosci [Suppl] 9:176.
30. Katona I, Acsády L, Freund TF (1999) Postsynaptic targets of somatostatin-immunoreactive interneurons in the rat hippocampus. Neuroscience 88:37-55.
31. Kawaguchi Y, Kubota Y (1996) Physiological and morphological identification of somatostatin-or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16:2701-2715.
32. Kawaguchi Y, Kubota Y (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85:677-701.
33. Kawaguchi Y, Shindou T (1998) Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. J Neurosci 18:6963-6976.
34. Kerner JA, Standaert DG, Penney JBJ, Young AB, Landwehrmeyer GB (1997) Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Brain Res Mol Brain Res 48:259-269.
35. Kosaka T, Wu JY, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp Brain Res 71:388-398.
36. Köhler C, Chan-Palay V (1982) Somatostatin-like immunoreactive neurons in the hippocampus: an immunocytochemical study in the rat. Neurosci Lett 34:259-264.
37. Köhler C, Eriksson LG, Davies S, Chan-Palay V (1987) Co-localization of neuropeptide tyrosine and somatostatin immunoreactivity in neurons of individual subfields of the rat hippocampal region. Neurosci Lett 78:1-6.
38. Kunkel DD, Schwartzkroin PA (1988) Ultrastructural characterization and GAD co-localization of somatostatin-like immunoreactive neurons in CA1 of rabbit hippocampus. Synapse 2:371-381.
39. Lacaille JC, Williams S (1990) Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36:349-359.
40. Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993.
41. Lowenstein DH, Thomas MJ, Smith DH, McIntosh TK (1992) Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J Neurosci 12:4846-4853.
42. h) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol (Lond) 497:119-130.
43. Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301-304.
44. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209-213.
45. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
46. Martin LJ, Blackstone CD, Huganir RL, Price DL (1992) Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9:259-270.
47. 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.
48. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences etween somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
49. Milner TA, Bacon CE (1989) Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus. J Comp Neurol 290:544-560.
50. Mizukawa K, Otsuka N, McGeer PL, Vincent SR, McGeer EG (1988) The ultrastructure of somatostatin-immunoreactive cell bodies, nerve fibers and terminals in the dorsal horn of rat spinal cord. Arch Histol Cytol 51:443-452.
51. Morise H, Shimomura O, Johnson FH, Winant J (1974) Intermolecular energy transfer in the bioluminescent system of Aequorea. Biochemistry 13:2656-2662.
52. Morrison JH, Benoit R, Magistretti PJ, Ling N, Bloom FE (1982) Immunohistochemical distribution of pro-somatostatin-related peptides in hippocampus. Neurosci Lett 34:137-142.
53. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
54. Naus CC, Morrison JH, Bloom FE (1988) Development of somatostatin-containing neurons and fibers in the rat hippocampus. Brain Res 468:113-121.
55. Oliva Jr AA, Smith KL, Swann JW (1998) Transgenic mice that express green fluorescent protein (GFP) in GABAergic neurons: a new tool for studying hippocampal interneurons. Soc Neurosci Abstr 24:1159.
56. Parra P, Gulyás AI, Miles R (1998) How many subtypes of inhibitory cells in the hippocampus? Neuron 20:983-993.
57. Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ (1992) Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111:229-233.
58. Roberts GW, Crow TJ, Polak JM (1985) Location of neuronal tangles in somatostatin neurones in Alzheimer's disease. Nature 314:92-94.
59. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Plainview, NY: Cold Spring Harbor Laboratory.
60. Sík A, Ylinen A, Penttonen M, Buzsáki G (1994) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 265:1722-1724.
61. Sík A, Penttonen M, Ylinen A, Buzsáki G (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15:6651-6665.
62. Sík A, Penttonen M, Buzsáki G (1997) Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur J Neurosci 9:573-588.
63. Sloviter RS (1987) Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73-76.
64. Sloviter RS (1991) Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41-66.
65. Sloviter RS, Lowenstein DH (1992) Heat shock protein expression in vulnerable cells of the rat hippocampus as an indicator of excitation-induced neuronal stress. J Neurosci 12:3004-3009.
66. Sloviter RS, Nilaver G (1987) Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neurol 256:42-60.
67. Szabó G, Katarova Z, Körtvély E, Greenspan RJ, Urbán Z (1996) Structure and the promoter region of the mouse gene encoding the 67-kD form of glutamic acid decarboxylase. DNA Cell Biol 15:1081-1091.
68. 28k -containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
69. Tóth 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.
70. Traub RD, Jefferys JG, Miles R, Whittington MA, Toth K (1994) A branching dendritic model of a rodent CA3 pyramidal neurone. J Physiol (Lond) 481:79-95.
71. Van Uden E, Veinbergs I, Mallory M, Orlando R, Masliah E (1999) A novel role for receptor-associated protein in somatostatin modulation: implications for Alzheimer's disease. Neuroscience 88:687-700.
72. Wonnacott T, Wonnacott R (1984) Introductory statistics for business and economics. New York: Wiley.
73. Yanagawa Y, Kobayashi T, Kamei T, Ishii K, Nishijima M, Takaku A, Tamura S (1997) Structure and alternative promoters of the mouse glutamic acid decarboxylase 67 gene. Biochem J 326:573-578.
74. Yanovsky Y, Sergeeva OA, Freund TF, Haas HL (1997) Activation of interneurons at the stratum oriens/alveus border suppresses excitatory transmission to apical dendrites in the CA1 area of the mouse hippocampus. Neuroscience 77:87-96.