Differential expression of intrinsic membrane currents in defined cell types of the anterolateral bed nucleus of the stria terminalis

Journal of Neurophysiology

Volumn 98, Issue 2, 2007, Pages 638-656

  Hammack, Sayamwong E ^a   Mania, Irakli ^a   Rainnie, Donald G ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; POTASSIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELL NUCLEUS; CELL TYPE; CONTROLLED STUDY; DEPOLARIZATION; HYPERPOLARIZATION; MALE; MEMBRANE CURRENT; NERVE CELL; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; STRIA TERMINALIS;

4-AMINOPYRIDINE; AGING; ANIMALS; BENZYLAMINES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GABA AGENTS; MALE; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; POTASSIUM CHANNEL BLOCKERS; QUINOXALINES; RATS; SEPTAL NUCLEI; SODIUM CHANNEL BLOCKERS; TETRAETHYLAMMONIUM; TETRODOTOXIN;

EID: 34547741600     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00382.2007     Document Type: Article

References (116)

1. Adamec R. The relationship between the amygdala and bed nucleus of the stria terminalis in the cat: an evoked potential and single cell study. Behav Neural Biol 52: 295-320, 1989.
2. Aghajanian GK. Modulation of a transient outward current in serotonergic neurones by alpha 1-adrenoceptors. Nature 315: 501-503, 1985.
3. Agrawal N, Hamam BN, Magistretti J, Alonso A, Ragsdale DS. Persistent sodium channel activity mediates subthreshold membrane potential oscillations and low-threshold spikes in rat entorhinal cortex layer V neurons. Neuroscience 102: 53-64, 2001.
4. Alheid GF. Extended amygdala and basal forebrain. Ann NY Acad Sci 985: 185-205, 2003.
5. Alheid GF, Heimer L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27: 1-39, 1988.
6. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-177, 1989.
7. Altomare C, Terragni B, Brioschi C, Milanesi R, Pagliuca C, Viscomi C, Moroni A, Baruscotti M, DiFrancesco D. Heteromeric HCN1-HCN4 channels: a comparison with native pacemaker channels from the rabbit sinoatrial node. J Physiol 549: 347-359, 2003.
8. Amir S, Lamont EW, Robinson B, Stewart J. A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J Neurosci 24: 781-790, 2004.
9. Amitai Y. Membrane potential oscillations underlying firing patterns in neocortical neurons. Neuroscience 63: 151-161, 1994.
10. Aracri P, Colombo E, Mantegazza M, Scalmani P, Curia G, Avanzini G, Franceschetti S. Layer-specific properties of the persistent sodium current in sensorimotor cortex. J Neurophysiol 95: 3460-3468, 2006.
11. Arluison M, Brochier G, Vankova M, Leviel V, Villalobos J, Tramu G. Demonstration of peptidergic afferents to the bed nucleus of the stria terminalis using local injections of colchicine. A combined immunohistochemical and retrograde tracing study. Brain Res Bull 34: 319-337, 1994.
12. Aston-Jones G, Harris GC. Brain substrates for increased drug seeking during protracted withdrawal. Neuropharmacology 47, Suppl. 1: 167-179, 2004.
13. Baraban SC, Tallent MK. Interneuron diversity series: interneuronal neuropeptides - endogenous regulators of neuronal excitability. Trends Neurosci 27: 135-142, 2004.
14. Boudaba C, Szabo K, Tasker JG. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16: 7151-7160, 1996.
15. Buisson B, Bottari SP, de Gasparo M, Gallo-Payet N, Payet MD. The angiotensin AT2 receptor modulates T-type calcium current in non-differentiated NG108-15 cells. FEBS Lett 309: 161-164, 1992.
16. Burdakov D, Ashcroft FM. Cholecystokinin tunes firing of an electrically distinct subset of arcuate nucleus neurons by activating A-type potassium channels. J Neurosci 22: 6380-6387, 2002.
17. Cardenas CG, Mar LP, Vysokanov AV, Arnold PB, Cardenas LM, Surmeier DJ, Scroggs RS. Serotonergic modulation of hyperpolarization-activated current in acutely isolated rat dorsal root ganglion neurons. J Physiol 518: 507-523, 1999.
18. Carr DB, Cooper DC, Ulrich SL, Spruston N, Surmeier DJ. Serotonin receptor activation inhibits sodium current and dendritic excitability in prefrontal cortex via a protein kinase C-dependent mechanism. J Neurosci 22: 6846-6855, 2002.
19. Casada JH, Dafny N. Restraint and stimulation of bed nucleus of the stria terminalis produce similar stress-like behaviors. Brain Res Bull 27: 207-212, 1991.
20. Casada JH, Dafny N. Evidence for two different afferent pathways carrying stress-related information (noxious and amygdala stimulation) to the bed nucleus of the stria terminalis. Brain Res 579: 93-98, 1992.
21. Casada JH, Dafny N. Responses of neurons in bed nucleus of the stria terminalis to microiontophoretically applied morphine, norepinephrine and acetylcholine. Neuropharmacology 32: 279-284, 1993.
22. 2+ channels. Annu Rev Cell Dev Biol 16: 521-555, 2000.
23. Chen S, Wang J, Siegelbaum SA. Properties of hyperpolarization- activated pacemaker current defined by coassembly of HCN1 and HCN2 subunits and basal modulation by cyclic nucleotide. J Gen Physiol 117: 491-504, 2001.
24. Crill WE. Persistent sodium current in mammalian central neurons. Annu Rev Physiol 58: 349-362, 1996.
25. Dalsass M, Siegel A. The bed nucleus of the stria terminalis: electrophysiological properties and responses to amygdaloid and hypothalamic stimulation. Brain Res 425: 346-350, 1987.
26. Dalsass M, Siegel A. Opioid peptide regulation of neurons in the bed nucleus of the stria terminalis: a microiontophoretic study. Brain Res 531: 346-349, 1990.
27. + channel: expression cloning and molecular properties. Proc Natl Acad Sci USA 90: 10235-10239, 1993.
28. Day M, Carr DB, Ulrich S, Ilijic E, Tkatch T, Surmeier DJ. Dendritic excitability of mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2, and Kleak channels. J Neurosci 25: 8776-8787, 2005.
29. De Jeu M, Geurtsen A, Pennartz C. A Ba(2+)-sensitive K(+) current contributes to the resting membrane potential of neurons in rat suprachiasmatic nucleus. J Neurophysiol 88: 869-878, 2002.
30. De Olmos JS, Alheid GF, Beltramino CA. Amygdala. In: The Rat Nervous System: Forebrain and Midbrain, edited by Paxinos G. New York: Academic Press, 1985, vol. 1, p. 223.
31. Dong HW, Petrovich GD, Swanson LW. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38: 192-246, 2001.
32. Dumont EC, Williams JT. Noradrenaline triggers GABAA inhibition of bed nucleus of the stria terminalis neurons projecting to the ventral tegmental area. J Neurosci 24: 8198-8204, 2004.
33. Egli RE, Kash TL, Choo K, Savchenko V, Matthews RT, Blakely RD, Winder DG. Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis. Neuropsychopharmacology 30: 657-668, 2005.
34. Egli RE, Winder DG. Dorsal and ventral distribution of excitable and synaptic properties of neurons of the bed nucleus of the stria terminalis. J Neurophysiol 90: 405-414, 2003.
35. Erb S, Stewart J. A role for the bed nucleus of the stria terminalis, but not the amygdala, in the effects of corticotropin-releasing factor on stress-induced reinstatement of cocaine seeking. J Neurosci 19: RC35, 1999.
36. Farley J, Auerbach S. Protein kinase C activation induces conductance changes in Hermissenda photoreceptors like those seen in associative learning. [Erratum appears in Nature 1986 Dec 18-31;324(6098):702]. Nature 319: 220-223, 1986.
37. Fisher R, Johnston D. Differential modulation of single voltage-gated calcium channels by cholinergic and adrenergic agonists in adult hippocampal neurons. J Neurophysiol 64: 1291-1302, 1990.
38. Franqueza L, Valenzuela C, Eck J, Tamkun MM, Tamargo J, Snyders DJ. Functional expression of an inactivating potassium channel (Kv4.3) in a mammalian cell line. Cardiovasc Res 41: 212-219, 1999.
39. Fraser DD, MacVicar BA. Low-threshold transient calcium current in rat hippocampal lacunosum-moleculare interneurons: kinetics and modulation by neurotransmitters. J Neurosci 11: 2812-2820, 1991.
40. Georges F, Aston-Jones G. Activation of ventral tegmental area cells by the bed nucleus of the stria terminalis: a novel excitatory amino acid input to midbrain dopamine neurons. J Neurosci 22: 5173-5187, 2002.
41. Goldin AL. Resurgence of sodium channel research. Annu Rev Physiol 63: 871-894, 2001.
42. Gorelova NA, Yang CR. Dopamine D1/D5 receptor activation modulates a persistent sodium current in rat prefrontal cortical neurons in vitro. J Neurophysiol 84: 75-87, 2000.
43. Gray TS, Magnuson DJ. Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides 13: 451-460, 1992.
44. Gutman GA, Chandy KG, Grissmer S, Lazdunski M, McKinnon D, Pardo LA, Robertson GA, Rudy B, Sanguinetti MC, Stuhmer W, Wang X. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev 57: 473-508, 2005.
45. Hammack SE, Guo J, Hazra R, Rainnie DG. Subthreshold intrinsic membrane currents actively modulate the firing properties of neurons in the anterolateral group of the bed nucleus of the stria terminalis (BNST). Proc Soc Neurosci, Atlanta, GA, 2006.
46. Hammack SE, Haensly JW, Rainnie DG. Activation of 5-HT7 receptors mediates a depolarizing response in a subset of neurons in the anterolateral cell group of the bed nucleus of the stria terminalis. Proc Soc Neurosci, Washington, DC, 2005.
47. Hammack SE, Richey KJ, Watkins LR, Maier SF. Chemical lesion of the bed nucleus of the stria terminalis blocks the behavioral consequences of uncontrollable stress. Behav Neurosci 118: 443-448, 2004.
48. Hartmann HA, Colom LV, Sutherland ML, Noebels JL. Selective localization of cardiac SCN5A sodium channels in limbic regions of rat brain. Nat Neurosci 2: 593-595, 1999.
49. Harvey PJ, Li X, Li Y, Bennett DJ. 5-HT2 receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 96: 1158-1170, 2006.
50. Herbison AE, Pape JR, Simonian SX, Skynner MJ, Sim JA. Molecular and cellular properties of GnRH neurons revealed through transgenics in the mouse. Mol Cell Endocrinol 185: 185-194, 2001.
51. Ho K, Nichols CG, Lederer WJ, Lytton J, Vassilev PM, Kanazirska MV, Hebert SC. Cloning and expression of an inwardly rectifying ATP-regulated potassium channel. Nature 362: 31-38, 1993.
52. Hur EE, Zaborszky L. Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization. J Comp Neurol 483: 351-373, 2005.
53. + channel Kir2.3 is localized at the postsynaptic membrane of excitatory synapses. Am J Physiol Cell Physiol 282: C1396-C1403, 2002.
54. Ingram CD, Cutler KL, Wakerley JB. Oxytocin excites neurones in the bed nucleus of the stria terminalis of the lactating rat in vitro. Brain Res 527: 167-170, 1990.
55. Isomoto S, Kondo C, Kurachi Y. Inwardly rectifying potassium channels: their molecular heterogeneity and function. Jpn J Physiol 47: 11-39, 1997.
56. Jasnow AM, Davis M, Huhman KL. Involvement of central amygdalar and bed nucleus of the stria terminalis corticotropin-releasing factor in behavioral responses to social defeat. Behav Neurosci 118: 1052-1061, 2004.
57. Ju G, Swanson LW, Simerly RB. Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: II. Chemoarchitecture. J Comp Neurol 280: 603-621, 1989.
58. Kaneda M, Kaneko A. Voltage-gated sodium currents in isolated retinal ganglion cells of the cat: relation between the inactivation kinetics and the cell type. Neurosci Res 11: 261-275, 1991.
59. + channel mRNAs are differentially expressed in the adult rat brain. J Neurosci 16: 3559-3570, 1996.
60. Klockner U, Lee JH, Cribbs LL, Daud A, Hescheler J, Pereverzev A, Perez-Reyes E, Schneider T. Comparison of the Ca2+ currents induced by expression of three cloned alpha1 subunits, alpha1G, alpha1H and alpha1I, of low-voltage-activated T-type Ca2+ channels. Eur J Neurosci 11: 4171-4178, 1999.
61. Larriva-Sahd J. Juxtacapsular nucleus of the stria terminalis of the adult rat: extrinsic inputs, cell types, and neuronal modules: a combined Golgi and electron microscopic study. J Comp Neurol 475: 220-237, 2004.
62. Larriva-Sahd J. Histological and cytological study of the bed nuclei of the stria terminalis in adult rat. II. Oval nucleus: extrinsic inputs, cell types, neuropil, and neuronal modules. J Comp Neurol 497: 772-807, 2006.
63. Lechner SM, Valentino RJ. Glucocorticoid receptor-immunoreactivity in corticotrophin-releasing factor afferents to the locus coeruleus. Brain Res 816: 17-28, 1999.
64. Lee JH, Gomora JC, Cribbs LL, Perez-Reyes E. Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H. Biophys J 77: 3034-3042, 1999.
65. Lenglet S, Louiset E, Delarue C, Vaudry H, Contesse V. Activation of 5-HT(7) receptor in rat glomerulosa cells is associated with an increase in adenylyl cyclase activity and calcium influx through T-type calcium channels. Endocrinology 143: 1748-1760, 2002.
66. Levita L, Hammack SE, Mania I, Li XY, Davis M, Rainnie DG. 5-Hydroxytryptamine1A-like receptor activation in the bed nucleus of the stria terminalis: electrophysiological and behavioral studies. Neuroscience 128: 583-596, 2004.
67. Llinas RR, Steriade M. Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95: 3297-3308, 2006.
68. + currents in callosal-projecting rat visual cortical neurons. J Neurophysiol 78: 2309-2320, 1997.
69. Ludwig A, Zong X, Jeglitsch M, Hofmann F, Biel M. A family of hyperpolarization-activated mammalian cation channels. Nature 393: 587-591, 1998.
70. Marchetti C, Carbone E, Lux HD. Effects of dopamine and noradrenaline on Ca channels of cultured sensory and sympathetic neurons of chick. Pflügers Arch/Eur J Physiol 406: 104-111, 1986.
71. Martina M, Royer S, Paré D. Physiological properties of central medial and central lateral amygdala neurons. J Neurophysiol 82: 1843-1854, 1999.
72. Maurice N, Tkatch T, Meisler M, Sprunger LK, Surmeier DJ. D1/D5 dopamine receptor activation differentially modulates rapidly inactivating and persistent sodium currents in prefrontal cortex pyramidal neurons. J Neurosci 21: 2268-2277, 2001.
73. McCormick DA, Pape HC. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol 431: 291-318, 1990.
74. McDonald AJ. Neurons of the bed nucleus of the stria terminalis: a Golgi study in the rat. Brain Res Bull 10: 111-120, 1983.
75. Mistrik P, Mader R, Michalakis S, Weidinger M, Pfeifer A, Biel M. The murine HCN3 gene encodes a hyperpolarization-activated cation channel with slow kinetics and unique response to cyclic nucleotides. J Biol Chem 280: 27056-27061, 2005.
76. Monteggia LM, Eisch AJ, Tang MD, Kaczmarek LK, Nestler EJ. Cloning and localization of the hyperpolarization-activated cyclic nucleotide-gated channel family in rat brain. Brain Res Mol Brain Res 81: 129-139, 2000.
77. Morris NP, Fyffe RE, Robertson B. Characterisation of hyperpolarization-activated currents (I(h)) in the medial septum/diagonal band complex in the mouse. Brain Res 1006: 74-86, 2004.
78. Nakajima Y, Nakajima S, Leonard RJ, Yamaguchi K. Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc Natl Acad Sci USA 83: 3022-3026, 1986.
79. Nelson S. Cortical microcircuits: diverse or canonical? Neuron 36: 19-27, 2002.
80. Newman SW. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann NY Acad Sci 877: 242-257, 1999.
81. Nichols CG, Lopatin AN. Inward rectifier potassium channels. Annu Rev Physiol 59: 171-191, 1997.
82. Nisenbaum ES, Wilson CJ. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 15: 4449-4463, 1995.
83. Perez-Reyes E. Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83: 117-161, 2003.
84. Peruzzi D, Sivaramakrishnan S, Oliver DL. Identification of cell types in brain slices of the inferior colliculus. Neuroscience 101: 403-416, 2000.
85. Placantonakis DG, Schwarz C, Welsh JP. Serotonin suppresses subthreshold and suprathreshold oscillatory activity of rat inferior olivary neurones in vitro. J Physiol 524: 833-851, 2000.
86. Qiu DL, Chu CP, Shirasaka T, Tsukino H, Nakao H, Kato K, Kunitake T, Katoh T, Kannan H. Corticotrophin-releasing factor augments the I(H) in rat hypothalamic paraventricular nucleus parvocellular neurons in vitro. J Neurophysiol 94: 226-234, 2005.
87. Qiu J, Bosch MA, Jamali K, Xue C, Kelly MJ, Ronnekleiv OK. Estrogen upregulates T-type calcium channels in the hypothalamus and pituitary. J Neurosci 26: 11072-11082, 2006.
88. Rainnie DG. Neurons of the bed nucleus of the stria terminalis (BNST). Electrophysiological properties and their response to serotonin. Ann NY Acad Sci 877: 695-699, 1999.
89. Rainnie DG, Bergeron R, Sajdyk TJ, Patil M, Gehlert DR, Shekhar A. Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 24: 3471-3479, 2004.
90. Roberts L, Greene JR. Hyperpolarization-activated current (Ih): a characterization of subicular neurons in brain slices from socially and individually housed rats. Brain Res 1040: 1-13, 2005.
91. + channels: more than model behaviour. Trends Pharmacol Sci 18: 474-483, 1997.
92. Robinson RB, Siegelbaum SA. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65: 453-480, 2003.
93. Rudy B. Diversity and ubiquity of K channels. Neuroscience 25: 729-749, 1988.
94. Ryu PD, Randic M. Low- and high-voltage-activated calcium currents in rat spinal dorsal horn neurons. J Neurophysiol 63: 273-285, 1990.
95. Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20: 5264-5275, 2000.
96. Santoro B, Liu DT, Yao H, Bartsch D, Kandel ER, Siegelbaum SA, Tibbs GR. Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell 93: 717-729, 1998.
97. Saraga F, Skinner FK. Dynamics and diversity in interneurons: a model exploration with slowly inactivating potassium currents. Neuroscience 113: 193-203, 2002.
98. + (A-type) currents in rat brain. J Neurophysiol 79: 1081-1091, 1998.
99. Shimada S, Inagaki S, Kubota Y, Ogawa N, Shibasaki T, Takagi H. Coexistence of peptides (corticotropin releasing factor/neurotensin and substance P/somatostatin) in the bed nucleus of the stria terminalis and central amygdaloid nucleus of the rat. Neuroscience 30: 377-383, 1989.
100. + currents in neurons. Neurosci Res 42: 7-14, 2002.
101. Stafstrom CE, Schwindt PC, Chubb MC, Crill WE. Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol 53: 153-170, 1985.
102. 2+. J Physiol 475: 1-7, 1994.
103. Sun N, Cassell MD. Intrinsic GABAergic neurons in the rat central extended amygdala. J Comp Neurol 330: 381-404, 1993.
104. + channels in rat hippocampal pyramidal cells. J Physiol 539: 67-75, 2002.
105. Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, Bayliss DA. Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19: 1895-1911, 1999.
106. + channel alpha subunit. FEBS Lett 400: 215-220, 1997.
107. Urbani A, Belluzzi O. Riluzole inhibits the persistent sodium current in mammalian CNS neurons. Eur J Neurosci 12: 3567-3574, 2000.
108. Varga AW, Yuan LL, Anderson AE, Schrader LA, Wu GY, Gatchel JR, Johnston D, Sweatt JD. Calcium-calmodulin-dependent kinase II modulates Kv4.2 channel expression and upregulates neuronal A-type potassium currents. J Neurosci 24: 3643-3654, 2004.
109. Vega-Saenz de Miera EC, Rudy B, Sugimori M, Llinas R. Molecular characterization of the sodium channel subunits expressed in mammalian cerebellar Purkinje cells. Proc Natl Acad Sci USA 94: 7059-7064, 1997.
110. Veinante P, Stoeckel ME, Freund-Mercier MJ. GABA- and peptide-immunoreactivities co-localize in the rat central extended amygdala. Neuroreport 8: 2985-2989, 1997.
111. Walker DL, Davis M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17: 9375-9383, 1997.
112. Walker DL, Toufexis DJ, Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463: 199-216, 2003.
113. Wang WT, Wan YH, Zhu JL, Lei GS, Wang YY, Zhang P, Hu SJ. Theta-frequency membrane resonance and its ionic mechanisms in rat subicular pyramidal neurons. Neuroscience 140: 45-55, 2006.
114. Woodhams PL, Roberts GW, Polak JM, Crow TJ. Distribution of neuropeptides in the limbic system of the rat: the bed nucleus of the stria terminalis, septum and preoptic area. Neuroscience 8: 677-703, 1983.
115. Wu J, Hablitz JJ. Cooperative activation of D1 and D2 dopamine receptors enhances a hyperpolarization-activated inward current in layer I interneurons. J Neurosci 25: 6322-6328, 2005.
116. Wu N, Enomoto A, Tanaka S, Hsiao CF, Nykamp DQ, Izhikevich E, Chandler SH. Persistent sodium currents in mesencephalic v neurons participate in burst generation and control of membrane excitability. J Neurophysiol 93: 2710-2722, 2005.