GABA excitation in mouse hilar neuropeptide Y neurons

Journal of Physiology

Volumn 579, Issue 2, 2007, Pages 445-464

  Fu, Li Ying ^a   van den Pol, Anthony N ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; BICUCULLINE; CALCIUM ION; GRAMICIDIN; MAGNESIUM ION; MUSCIMOL; NEUROPEPTIDE Y; SOMATOSTATIN; TETRODOTOXIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; GREEN FLUORESCENT PROTEIN;

4 AMINOBUTYRIC ACID RELEASE; AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL ADHESION; CONTROLLED STUDY; DENTATE NUCLEUS; ELECTRIC RESISTANCE; HIPPOCAMPUS; HYPERPOLARIZATION; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL INHIBITION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NERVE POTENTIAL; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC INHIBITION; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN SECRETION; SOLUTION AND SOLUBILITY; SOMATOSTATIN RELEASE; SPIKE WAVE; ANIMAL CELL; ANIMAL EXPERIMENT; BRAIN CELL; BRAIN CORTEX; BRAIN REGION; CELL COUNT; CELL SHAPE; CELL SIZE; DENDRITIC CELL; GRANULE CELL; HIPPOCAMPAL CA3 REGION; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION;

ANIMALS; BICUCULLINE; EVOKED POTENTIALS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INTERNEURONS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NEUROPEPTIDE Y; PATCH-CLAMP TECHNIQUES; PICROTOXIN; RECEPTORS, GABA-A; SOMATOSTATIN;

EID: 33847662813     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.019356     Document Type: Article

References (90)

1. Acsády L, Kamondi A, Sik A, Freund T & Buzsaki G (1998). GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J Neurosci 18, 3386-3403.
2. Acuna-Goycolea C, Tamamaki N, Yanagawa Y, Obata K & van den Pol AN (2005). Mechanisms of neuropeptide Y, peptide YY, and pancreatic polypeptide inhibition of identified green fluorescent protein-expressing GABA neurons in the hypothalamic neuroendocrine arcuate nucleus. J Neurosci 25, 7406-7419.
3. Akaike N (1996). Gramicidin perforated patch recording and intracellular chloride activity in excitable cells. Prog Biophys Mol Biol 65, 251-264. Review.
4. Alger B & Nicoll R (1982). Pharmacological evidence for two kinds of GABA receptor on rat hippocampal pyramidal cells studied in vitro. J Physiol 328, 125-141.
5. Amaral DG (1978). A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182, 851-914.
6. Baraban SC, Hollopeter G, Erickson JC, Schwartzkroin PA & Palmiter RD (1997). Knock-out mice reveal a critical antiepileptic role for neuropeptide Y. J Neurosci 17, 8927-8936.
7. Barker JL, McBurney RN & Mathers DA (1983). Convulsant-induced depression of amino acid responses in cultured mouse spinal neurones studied under voltage clamp. Br J Pharmacol 80, 619-629.
8. Ben-Ari Y, Cherubini E, Corradetti R & Gaiarsa JL (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416, 303-325.
9. Ben-Ari Y, Tseeb V, Raggozzino D, Khazipov R & Gaiarsa JL (1994). Gamma-a minobutyric acid (GABA): A fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog Brain Res 102, 261-273.
10. Boehm S & Betz H (1997). Somatostatin inhibits excitatory transmission at rat hippocampal synapses via presynaptic receptors. J Neurosci 17, 4066-4075.
11. Buckmaster PS & Dudek FE (1997). Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385, 385-404.
12. Buckmaster PS, Otero-Corchon V, Rubinstein M & Low MJ (2002). Heightened seizure severity in somatostatin knockout mice. Epilepsy Res 48, 43-56.
13. Buckmaster PS & Schwartzkroin PA (1995). Interneurons and inhibition in the dentate gyrus of the rat in vivo. J Neurosci 15, 774-789.
14. Chan-Palay V (1987). Somatostatin immunoreactive neurons in the human hippocampus and cortex shown by immunogold/silver intensification on vibratome sections: Coexistence with neuropeptide Y neurons, and effects in Alzheimer-type dementia. J Comp Neurol 260, 201-223.
15. Chen G, Trombley PQ & van den Pol AN (1996). Excitatory actions of GABA in developing rat hypothalamic neurones. J Physiol 494, 451-464.
16. Clements JD & Bekkers JM (1997). Detection of spontaneous synaptic events with an optimally scaled template. Biophys J 73, 220-229.
17. Colmers WF, Klapstein GJ, Fournier A, St-Pierre S & Treherne KA (1991). Presynaptic inhibition by neuropeptide Y in rat hippocampal slice in vitro is mediated by a Y2 receptor. Br J Pharmacol 102, 41-44.
18. Colmers WF, Lukowiak K & Pittman QJ (1987). Presynaptic action of neuropeptide Y in area CA1 of the rat hippocampal slice. J Physiol 383, 285-299.
19. Constanti A (1978). The 'mixed' effect of picrotoxin on the GABA dose/ conductance relation recorded from lobster muscle. Neuropharmacology 17, 159-167.
20. Debarbieux F, Brunton J & Charpak S (1998). Effect of bicuculline on thalamic activity: A direct blockade of IAHP in reticularis neurons. J Neurophysiol 79, 2911-2918.
21. de Lanerolle NC, Kim JH, Robbins RJ & Spencer DD (1989). Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495, 387-395.
22. Deller T & Leranth C (1990). Synaptic connections of neuropeptide Y (NPY) immunoreactive neurons in the hilar area of the rat hippocampus. J Comp Neurol 300, 433-447.
23. Dreifuss JJ, Kalnins I, Kelly JS, Ruf KB (1971). Action potentials and release of neurohypophysial harmones in vitro. J Physiol 215, 805-817.
24. Dutton A, Dyball RE (1979). Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol 290, 433-440.
25. Erickson JC, Clegg KE & Palmiter RD (1996). Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381, 415-421.
26. 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.
27. Forti M & Michelson HB (1998). Synaptic connectivity of distinct hilar interneuron subpopulations. J Neurophysiol 79, 3229-3237.
28. Freund TF & Buzsaki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
29. Fu LY, Acuna-Goycolea C & van den Pol AN (2004). Neuropeptide Y inhibits hypocretin/orexin neurons by multiple presynaptic and postsynaptic mechanisms: Tonic depression of the hypothalamic arousal system. J Neurosci 24, 8741-8751.
30. Gao XB, Chen G & van den Pol AN (1998). GABA-dependent firing of glutamate-evoked action potentials at AMPA/kainate receptors in developing hypothalamic neurons. J Neurophysiol 79, 716-726.
31. Gulledge AT & Stuart GJ (2003). Excitatory actions of GABA in the cortex. Neuron 37, 299-309.
32. Gulyas AI, 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.
33. 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.
34. Hajos N, Acsady L & Freund TF (1996). Target selectivity and neurochemical characteristics of VIP-immunoreactive interneurons in the rat dentate gyrus. Eur J Neurosci 8, 1415-1431.
35. Hara M, Inoue M, Yasukura T, Ohnishi S, Mikami Y & Inagaki C (1992). Uneven distribution of intracellular Cl- in rat hippocampal neurons. Neurosci Lett 143, 135-138.
36. Hsu M & Buzsaki G (1993). Vulnerability of mossy fiber targets in the rat hippocampus to forebrain ischemia. J Neurosci 13, 3964-3979.
37. Johansen FF, Zimmer J & Diemer NH (1987). Early loss of somatostatin neurons in dentate hilus after cerebral ischemia in the rat precedes CA-1 pyramidal cell loss. Acta Neuropathol 73, 110-114.
38. + transient. J Neurosci 17, 7662-7672.
39. Khawaled R, Bruening-Wright A, Adelman JP & Maylie J (1999). Bicuculline block of small-conductance calcium-activated potassium channels. Pflugers Arch 438, 314-321.
40. Khazipov R, Khalilov I, Tyzio R, Morozova E, Ben-Ari Y & Holmes GL (2004). Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur J Neurosci 19, 590-600.
41. Klapstein GJ & Colmers WF (1993). On the sites of presynaptic inhibition by neuropeptide Y in rat hippocampus in vitro. Hippocampus 3, 103-111.
42. Klapstein GJ & Colmers WF (1997). Neuropeptide Y suppresses epileptiform activity in rat hippocampus in vitro. J Neurophysiol 78, 1651-1661.
43. 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.
44. 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.
45. 2+ oscillations mediated by the synergistic excitatory actions of GABA A and NMDA receptors in the neonatal hippocampus. Neuron 18, 243-255.
46. Leranth C, Malcolm AJ & Frotscher M (1990). Afferent and efferent synaptic connections of somatostatin-immunoreactive neurons in the rat fascia dentata. J Comp Neurol 295, 111-122.
47. Li Y, Gao XB, Sakurai T & van den Pol AN (2002). Hypocretin/orexin excites hypocretin neurons via a local glutamate neuron-a potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36, 1169-1181.
48. Lübke J, Frotscher M & Spruston N (1998). Specialized electrophysiological properties of anatomically identified neurons in the hilar region of the rat fascia dentata. J Neurophysiol 79, 1518-1534.
49. Ma Y, Hu H, Berrebi AS, Mathers PH & Agmon A (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26, 5069-5082.
50. Mathern GW, Babb TL, Pretorius JK & Leite JP (1995). Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci 15, 3990-4004.
51. Mazarati AM & Telegdy G (1992). Effects of somatostatin and anti-somatostatin serum on picrotoxin-kindled seizures. Neuropharmacol 31, 793-797.
52. Mazarati A & Wasterlain CG (2002). Anticonvulsant effects of four neuropeptides in the rat hippocampus during self-sustaining status epilepticus. Neurosci Lett 331, 123-127.
53. A receptors in the hippocampus. Science 253, 1420-1423.
54. Michelson HB & Wong RK (1994). Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J Physiol 477, 35-45.
55. Milner TA & Veznedaroglu E (1993). Septal efferent axon terminals identified by anterograde degeneration show multiple sites for modulation of neuropeptide Y-containing neurons in the rat dentate gyrus. Synapse 14, 101-112.
56. Mitchell J, Cook I & Hervey V (1997). Effect of seizures on hippocampal peptidergic neurons. Neuropathol Appl Neurobiol 23, 299-306.
57. Mitchell J, Gatherer M & Sundstrom LE (1995). Loss of hilar somatostatin neurons following tetanus toxin-induced seizures. Acta Neuropathol 89, 425-430.
58. Moore SD, Madamba SG, Joels M & Siggins GR (1988). Somatostatin augments the M-current in hippocampal neurons. Science 239, 278-280.
59. Mott DD, Turner DA, Okazaki MM & Lewis DV (1997). Interneurons of the dentate-hilus border of the rat dentate gyrus: Morphological and electrophysiological heterogeneity. J Neurosci 17, 3990-4005.
60. Oliva AA Jr, 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.
61. Pare D, deCurtis M & Llinas R (1992). Role of the hippocampal-entorhinal loop in temporal lobe epilepsy: Extra- and intracellular study in the isolated guinea pig brain in vitro. J Neurosci 12, 1867-1881.
62. Paredes MF, Greenwood J & Baraban SC (2003). Neuropeptide Y modulates a G protein-coupled inwardly rectifying potassium current in the mouse hippocampus. Neurosci Lett 340, 9-12.
63. Parra P, Gulyas AI & Miles R (2000). How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983-993.
64. Patrylo PR, van den Pol AN, Spencer DD & Williamson A (1999). NPY inhibits glutamatergic excitation in the epileptic human dentate gyrus. J Neurophysiol 82, 478-483.
65. Perkins KL & Wong RK (1996). Ionic basis of the postsynaptic depolarizing GABA response in hippocampal pyramidal cells. J Neurophysiol 76, 3886-3894.
66. Robbins RJ, Brines ML, Kim JH, Adrian T, de Lanerolle N, Welsh S & Spencer DD (1991). A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy. Ann Neurol 29, 325-332.
67. Roseberry AG, Liu H, Jackson AC, Cai X & Friedman JM (2004). Neuropeptide Y-mediated inhibition of proopiomelanocortin neurons in the arcuate nucleus shows enhanced desensitization in ob/ob mice. Neuron 41, 711-722.
68. Scharfman HE (1991). Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 11, 1660-1673.
69. Scharfman HE & Sarvey JM (1987). Responses to GABA recorded from identified rat visual cortical neurons. Neuroscience 23, 407-422.
70. Schwarzer C, Williamson JM, Lothman EW, Vezzani A & Sperk G (1995). Somatostatin, neuropeptide Y, neurokinin B and cholecystokinin immunoreactivity in two chronic models of temporal lobe epilepsy. Neuroscience 69, 831-845.
71. + conductance in rat CA1 hippocampal neurons. J Neurophysiol 79, 1230-1238.
72. Sloviter RS (1987). Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235, 73-76.
73. Sperk G, Marksteiner J, Gruber B, Bellmann R, Mahata M & Ortler M (1992). Functional changes in neuropeptide Y- and somatostatin-containing neurons induced by limbic seizures in the rat. Neuroscience 50, 831-846.
74. 3-transport. J Physiol 519, 693-712.
75. A receptors. Science 269, 977-981.
76. Swann JW, Brady RJ & Martin DL (1989). Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 28, 551-561.
77. Tallent MK & Siggins GR (1999). Somatostatin acts in CA1 and CA3 to reduce hippocampal epileptiform activity. J Neurophysiol 81, 1626-1635.
78. Tu B, Timofeeva O, Jiao Y & Nadler JV (2005). Spontaneous release of neuropeptide Y tonically inhibits recurrent mossy fiber synaptic transmission in epileptic brain. J Neurosci 25, 1718-1729.
79. van den Pol AN, Acuna-Goycolea C, Clark KR & Ghosh PK (2004). Physiological properties of hypothalamic MCH neurons identified with selective expression of reporter gene after recombinant virus infection. Neuron 42, 635-652.
80. van den Pol AN, Ghosh PK, Liu RJ, Li Y, Aghajanian GK & Gao XB (2002). Hypocretin (orexin) enhances neuron activity and cell synchrony in developing mouse GFP-expressing locus coeruleus. J Physiol 541, 169-185.
81. Vezzani A, Sperk G & Colmers WF (1999). Neuropeptide Y: Emerging evidence for a functional role in seizure modulation. Trends Neurosci 22, 25-30.
82. van Vliet EA, Aronica E, Tolner EA, Lopes da Silva FH & Gorter JA (2004). Progression of temporal lobe epilepsy in the rat is associated with immunocytochemical changes in inhibitory interneurons in specific regions of the hippocampal formation. Exp Neurol 187, 367-379.
83. Wang YF, Gao XB & van den Pol AN (2001). Membrane properties underlying patterns of GABA-dependent action potentials in developing mouse hypothalamic neurons. J Neurophysiol 86, 1252-1265.
84. Wang HL, Reisine T & Dichter M (1990). Somatostatin-14 and somatostatin-28 inhibit calcium currents in rat neocortical neurons. Neuroscience 38, 335-342.
85. Woldbye DP, Larsen PJ, Mikkelsen JD, Klemp K, Madsen TM & Bolwig TG (1997). Powerful inhibition of kainic acid seizures by neuropeptide Y via Y5-like receptors. Nat Med 3, 761-764.
86. Woldbye DP, Madsen TM, Larsen PJ, Mikkelsen JD & Bolwig TG (1996). Neuropeptide Y inhibits hippocampal seizures and wet dog shakes. Brain Res 737, 162-168.
87. Wong RK & Watkins DJ (1982). Cellular factors influencing GABA response in hippocampal pyramidal cells. J Neurophysiol 48, 938-951.
88. Wong T, Zhang XL, Asl MN, Wu CP, Carlen PL & Zhang L (2005). Postnatal development of intrinsic GABAergic rhythms in mouse hippocampus. Neuroscience 134, 107-120.
89. Yamano M & Luiten PG (1989). Direct synaptic contacts of medial septal efferents with somatostatin immunoreactive neurons in the rat hippocampus. Brain Res Bull 22, 993-1001.
90. Yoon KW, Covey DF & Rothman SM (1993). Multiple mechanisms of picrotoxin block of GABA-induced currents in rat hippocampal neurons. J Physiol 464, 423-439.