Dopaminergic modulation of GABAergic transmission in the entorhinal cortex: Concerted roles of α1 adrenoreceptors, inward rectifier K+, and T-type Ca2+ channels

Cerebral Cortex

Volumn 24, Issue 12, 2014, Pages 3195-3208

  Cilz, Nicholas I ^a   Kurada, Lalitha ^a   Hu, Binqi ^a   Lei, Saobo ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Depolarization; Entorhinal; GABAA receptor; Interneuron; Synapse; Synaptic transmission

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR; AMPHETAMINE; CALCIUM CHANNEL T TYPE; DOPAMINE; INWARDLY RECTIFYING POTASSIUM CHANNEL; NORADRENALIN; 1,2-BIS(2-AMINOPHENOXY)ETHANE-N,N,N',N'-TETRAACETIC ACID; 4 AMINOBUTYRIC ACID; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM CHANNEL BLOCKING AGENT; CHELATING AGENT; EGTAZIC ACID; MIBEFRADIL; POTASSIUM CHANNEL BLOCKING AGENT;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL ACTIVATION; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; ENTORHINAL CORTEX; EXTRACELLULAR SPACE; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MEMBRANE DEPOLARIZATION; MEMBRANE STEADY POTENTIAL; NERVE POTENTIAL; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; ELECTROSTIMULATION; IN VITRO STUDY; METABOLISM; NERVE CELL; NERVE CELL INHIBITION; NEWBORN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, T-TYPE; CHELATING AGENTS; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; ELECTRIC STIMULATION; ENTORHINAL CORTEX; GAMMA-AMINOBUTYRIC ACID; IN VITRO TECHNIQUES; INHIBITORY POSTSYNAPTIC POTENTIALS; MIBEFRADIL; NEURAL INHIBITION; NEURONS; NEUROTRANSMITTER AGENTS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-1; SYNAPTIC TRANSMISSION;

EID: 84920855184     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht177     Document Type: Article

References (108)

1. Akil M, Lewis DA. 1993. The dopaminergic innervation of monkey entorhinal cortex. Cereb Cortex. 3:533-550.
2. Anfossi G, Massucco P, Mularoni E, Mattiello L, Cavalot F, Burzacca S, Trovati M. 1993. Effect of dopamine on adenosine 3', 5'-cyclic monophosphate levels in human platelets. Gen Pharmacol. 24:435-438.
3. Arnold SE, Hyman BT, Van Hoesen GW, Damasio AR. 1991. Some cytoarchitectural abnormalities of the entorhinal cortex in schizophrenia. Arch Gen Psychiatry. 48:625-632.
4. Avoli M, D'Antuono M, Louvel J, Kohling R, Biagini G, Pumain R, D'Arcangelo G, Tancredi V. 2002. Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol. 68:167-207.
5. 2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae I and II. J Neurosci. 18:8740-8750.
6. Barish ME. 1991. Increases in intracellular calcium ion concentration during depolarization of cultured embryonic Xenopus spinal neurones. J Physiol. 444:545-565.
7. Beaulieu JM, Gainetdinov RR. 2011. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev. 63:182-217.
8. Behr J, Gloveli T, Schmitz D, Heinemann U. 2000. Dopamine depresses excitatory synaptic transmission onto rat subicular neurons via presynaptic D1-like dopamine receptors. J Neurophysiol. 84:112-119.
9. Bessaih T, Leresche N, Lambert RC. 2008. T current potentiation increases the occurrence and temporal fidelity of synaptically evoked burst firing in sensory thalamic neurons. Proc Natl Acad Sci USA. 105:11376-11381.
10. Booze RM, Crisostomo EA, Davis JN. 1993. Beta-adrenergic receptors in the hippocampal and retrohippocampal regions of rats and guinea pigs: autoradiographic and immunohistochemical studies. Synapse. 13:206-214.
11. Boyajian CL, Loughlin SE, Leslie FM. 1987. Anatomical evidence for alpha-2 adrenoceptor heterogeneity: differential autoradiographic distributions of [3H]rauwolscine and [3H]idazoxan in rat brain. J Pharmacol Exp Ther. 241:1079-1091.
12. 2+]i through voltage-sensitive calcium channels. Eur J Neurosci. 10:971-975.
13. Carbone E, Marcantoni A, Giancippoli A, Guido D, Carabelli V. 2006. T-type channels-secretion coupling: evidence for a fast lowthreshold exocytosis. Pflugers Arch. 453:373-383.
14. Caruana DA, Chapman CA. 2008. Dopaminergic suppression of synaptic transmission in the lateral entorhinal cortex. Neural Plast. 2008:203514.
15. Caruana DA, Reed SJ, Sliz DJ, Chapman CA. 2007. Inhibiting dopamine reuptake blocks the induction of long-term potentiation and depression in the lateral entorhinal cortex of awake rats. Neurosci Lett. 426:6-11.
16. Caruana DA, Sorge RE, Stewart J, Chapman CA. 2006. Dopamine has bidirectional effects on synaptic responses to cortical inputs in layer II of the lateral entorhinal cortex. J Neurophysiol. 96:3006-3015.
17. Chee MJ, Price CJ, Statnick MA, Colmers WF. 2011. Nociceptin/orphanin FQ suppresses the excitability of neurons in the ventromedial nucleus of the hypothalamus. J Physiol. 589:3103-3114.
18. Cornil CA, Balthazart J, Motte P, Massotte L, Seutin V. 2002. Dopamine activates noradrenergic receptors in the preoptic area. J Neurosci. 22:9320-9330.
19. Cui RJ, Roberts BL, Zhao H, Zhu M, Appleyard SM. 2012. Serotonin activates catecholamine neurons in the solitary tract nucleus by increasing spontaneous glutamate inputs. J Neurosci. 32:16530-16538.
20. Cutsuridis V, Hasselmo M. 2012. GABAergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations. Hippocampus. 22:1597-1621.
21. Deng PY, Lei S. 2006. Bidirectional modulation of GABAergic transmission by cholecystokinin in hippocampal dentate gyrus granule cells of juvenile rats. J Physiol. 572:425-442.
22. Deng PY, Lei S. 2007. Long-term depression in identified stellate neurons of juvenile rat entorhinal cortex. J Neurophysiol. 97:727-737.
23. + channels. Mol Cell Neurosci. 39:273-284.
24. Deng PY, Porter JE, Shin HS, Lei S. 2006. Thyrotropin-releasing hormone increases GABA release in rat hippocampus. J Physiol. 577:497-511.
25. Deng PY, Xiao Z, Jha A, Ramonet D, Matsui T, Leitges M, Shin HS, Porter JE, Geiger JD, Lei S. 2010. Cholecystokinin facilitates glutamate release by increasing the number of readily releasable vesicles and releasing probability. J Neurosci. 30:5136-5148.
26. Deng PY, Xiao Z, Lei S. 2010. Distinct modes of modulation of GABA-ergic transmission by Group I metabotropic glutamate receptors in rat entorhinal cortex. Hippocampus. 20:980-993.
27. Dolcos F, La Bar KS, Cabeza R. 2005. Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proc Natl Acad Sci USA. 102:2626-2631.
28. Dong Y, Cooper D, Nasif F, Hu XT, White FJ. 2004. Dopamine modulates inwardly rectifying potassium currents in medial prefrontal cortex pyramidal neurons. J Neurosci. 24:3077-3085.
29. Erickson SL, Akil M, Levey AI, Lewis DA. 1998. Postnatal development of tyrosine hydroxylase- and dopamine transporter-immunoreactive axons in monkey rostral entorhinal cortex. Cereb Cortex. 8:415-427.
30. Falkai P, Bogerts B, Rozumek M. 1988. Limbic pathology in schizophrenia: the entorhinal region-a morphometric study. Biol Psychiatry. 24:515-521.
31. Fallon JH, Koziell DA, Moore RY. 1978. Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol. 180:509-532.
32. Ford CP, Phillips PE, Williams JT. 2009. The time course of dopamine transmission in the ventral tegmental area. J Neurosci. 29:13344-13352.
33. Gioanni Y, Thierry AM, Glowinski J, Tassin JP. 1998. Alpha1-adrenergic, D1, and D2 receptors interactions in the prefrontal cortex: implications for the modality of action of different types of neuroleptics. Synapse. 30:362-370.
34. Gorelova N, Seamans JK, Yang CR. 2002. Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol. 88:3150-3166.
35. Govindaiah G, Wang Y, Cox CL. 2010. Dopamine enhances the excitability of somatosensory thalamocortical neurons. Neuroscience. 170:981-991.
36. Haist F, Bowden Gore J, Mao H. 2001. Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nat Neurosci. 4:1139-1145.
37. Hamilton TJ, Wheatley BM, Sinclair DB, Bachmann M, Larkum ME, Colmers WF. 2010. Dopamine modulates synaptic plasticity in dendrites of rat and human dentate granule cells. Proc Natl Acad Sci USA. 107:18185-18190.
38. Hemby SE, Trojanowski JQ, Ginsberg SD. 2003. Neuron-specific age-related decreases in dopamine receptor subtype mRNAs. J Comp Neurol. 456:176-183.
39. Hidaka H. 1971. Fusaric (5-butylpicolinic) acid, an inhibitor of dopamine beta-hydroxylase, affects serotonin and noradrenaline. Nature. 231:54-55.
40. Huang Q, Zhou D, Chase K, Gusella JF, Aronin N, Di Figlia M. 1992. Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus. Proc Natl Acad Sci USA. 89:11988-11992.
41. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL. 1984. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science. 225:1168-1170.
42. Jensen LJ, Salomonsson M, Jensen BL, Holstein-Rathlou NH. 2004. Depolarization-induced calcium influx in rat mesenteric small arterioles is mediated exclusively via mibefradil-sensitive calcium channels. Br J Pharmacol. 142:709-718.
43. Joyal CC, Laakso MP, Tiihonen J, Syvalahti E, Vilkman H, Laakso A, Alakare B, Rakkolainen V, Salokangas RK, Hietala J. 2002. A volumetric MRI study of the entorhinal cortex in first episode neuroleptic-naive schizophrenia. Biol Psychiatry. 51:1005-1007.
44. Kassack MU, Höfgen B, Decker M, Eckstein N, Lehmann J. 2002. Pharmacological characterization of the benz[d]indolo[2, 3-g] azecine LE300, a novel type of a nanomolar dopamine receptor antagonist. Naunyn Schmiedebergs Arch Pharmacol. 366:543-550.
45. 2+ currents of odor sensitivity in olfactory receptor cells. J Neurosci. 21:RC144.
46. Kotzbauer PT, Trojanowsk JQ, Lee VM. 2001. Lewy body pathology in Alzheimer's disease. J Mol Neurosci. 17:225-232.
47. Kurian MA, Gissen P, Smith M, Heales S Jr, Clayton PT. 2011. The monoamine neurotransmitter disorders: an expanding range of neurological syndromes. Lancet Neurol. 10:721-733.
48. Kuzhikandathil EV, Oxford GS. 2002. Classic D1 dopamine receptor antagonist R-(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2, 3, 4, 5-tetrahydro-1H-3-benzazepine hydrochloride (SCH23390) directly inhibits G protein-coupled inwardly rectifying potassium channels. Mol Pharmacol. 62:119-126.
49. Lazou A, Markou T, Zioga M, Vasara E, Efstathiou A, Gaitanaki C. 2006. Dopamine mimics the cardioprotective effect of ischemic preconditioning via activation of alpha1-adrenoceptors in the isolated rat heart. Physiol Res. 55:1-8.
50. Lee TL, Hsu CT, Yen ST, Lai CW, Cheng JT. 1998. Activation of beta3-adrenoceptors by exogenous dopamine to lower glucose uptake into rat adipocytes. J Auton Nerv Syst. 74:86-90.
51. Leedham JA, Pennefather JN. 1986. Selectivities of some agonists acting at alpha 1- and alpha 2-adrenoreceptors in the rat vas deferens. J Auton Pharmacol. 6:39-46.
52. Lei S, Deng PY, Porter JE, Shin HS. 2007. Adrenergic facilitation of GABAergic transmission in rat entorhinal cortex. J Neurophysiol. 98:2868-2877.
53. Leviel V. 2011. Dopamine release mediated by the dopamine transporter, facts and consequences. J Neurochem. 118:475-489.
54. Lin Y, Quartermain D, Dunn AJ, Weinshenker D, Stone EA. 2008. Possible dopaminergic stimulation of locus coeruleus alpha1-adrenoceptors involved in behavioral activation. Synapse. 62:516-523.
55. Loretan K, Bissiere S, Luthi A. 2004. Dopaminergic modulation of spontaneous inhibitory network activity in the lateral amygdala. Neuropharmacology. 47:631-639.
56. 2+ currents in graded and spike-mediated synaptic transmission between leech heart interneurons. J Neurophysiol. 77:1779-1794.
57. Mayne EW, Craig MT, McBain CJ, Paulsen O. 2013. Dopamine suppresses persistent network activity via D (1)-like dopamine receptors in rat medial entorhinal cortex. Eur J Neurosci. 37:1242-1247.
58. 11C]talsupram: candidate PET ligands for the norepinephrine transporter. Nucl Med Biol. 31:705-718.
59. Munsch T, Yanagawa Y, Obata K, Pape HC. 2005. Dopaminergic control of local interneuron activity in the thalamus. Eur J Neurosci. 21:290-294.
60. Nagatsu T, Hidaka H, Kuzuya H, Takeya K, Umezawa H. 1970. Inhibition of dopamine beta-hydroxylase by fusaric acid (5-butylpicolinic acid) in vitro and in vivo. Biochem Pharmacol. 19:35-44.
61. Ooi H, Colucci WS. 2001. Pharmacological treatment of heart failure. In: Hardman JG, Limbird LE, Gilman AG editors. The pharmacological basis of therapeutics, 10th ed. New York: McGraw-Hill, p. 901.
62. Ouedraogo L, Magnon M, Sawadogo L, Tricoche R. 1998. Receptors involved in the positive inotropic action induced by dopamine on the ventricle of a 7-day-old chick embryo heart. Fundam Clin Pharmacol. 12:133-142.
63. Palkovits M, Zaborszky L, Brownstein MJ, Fekete MI, Herman JP, Kanyicska B. 1979. Distribution of norepinephrine and dopamine in cerebral cortical areas of the rat. Brain Res Bull. 4:593-601.
64. Pan ZH, Hu HJ, Perring P, Andrade R. 2001. T-type Ca (2+) channels mediate neurotransmitter release in retinal bipolar cells. Neuron. 32:89-98.
65. Phillips AG, Vacca G, Ahn S. 2008. A top-down perspective on dopamine, motivation and memory. Pharmacol Biochem Behav. 90:236-249.
66. + currents through a cAMP-dependent protein kinase A-independent mechanism. Neuroscience. 167:678-690.
67. Pralong E, Jones RS. 1993. Interactions of dopamine with glutamateand GABA-mediated synaptic transmission in the rat entorhinal cortex in vitro. Eur J Neurosci. 5:760-767.
68. Pralong E, Magistretti PJ. 1995. Noradrenaline increases K-conductance and reduces glutamatergic transmission in the mouse entorhinal cortex by activation of alpha 2-adrenoreceptors. Eur J Neurosci. 7:2370-2378.
69. Pralong E, Magistretti PJ. 1994. Noradrenaline reduces synaptic responses in normal and tottering mouse entorhinal cortex via alpha 2 receptors. Neurosci Lett. 179:145-148.
70. Prasad KM, Patel AR, Muddasani S, Sweeney J, Keshavan MS. 2004. The entorhinal cortex in first-episode psychotic disorders: a structural magnetic resonance imaging study. Am J Psychiatry. 161:1612-1619.
71. Rajfer SI, Borow KM, Lang RM, Neumann A, Carroll JD. 1988. Effects of dopamine on left ventricular afterload and contractile state in heart failure: relation to the activation of beta 1-adrenoceptors and dopamine receptors. J Am Coll Cardiol. 12:498-506.
72. 1A receptors. Neuropharmacology. 63:1218-1226.
73. 2+ signals mediated by alpha1B-adrenoceptors in rat pineal cells. Eur J Pharmacol. 430:9-17.
74. Richfield EK, Young AB, Penney JB. 1989. Comparative distributions of dopamine D-1 and D-2 receptors in the cerebral cortex of rats, cats, and monkeys. J Comp Neurol. 286:409-426.
75. Rivera A, Penafiel A, Megias M, Agnati LF, Lopez-Tellez JF, Gago B, Gutierrez A, de la Calle A, Fuxe K. 2008. Cellular localization and distribution of dopamine D (4) receptors in the rat cerebral cortex and their relationship with the cortical dopaminergic and noradrenergic nerve terminal networks. Neuroscience. 155:997-1010.
76. Robbins J, Wakakuwa K, Ikeda H. 1988. Noradrenaline action on cat retinal ganglion cells is mediated by dopamine (D2) receptors. Brain Res. 438:52-60.
77. Rosenkranz JA, Johnston D. 2006. Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex. J Neurosci. 26:3229-3244.
78. Rosenkranz JA, Johnston D. 2007. State-dependent modulation of amygdala inputs by dopamine-induced enhancement of sodium currents in layer V entorhinal cortex. J Neurosci. 27:7054-7069.
79. Rothman RB, Baumann MH, Dersch CM, Romero DV, Rice KC, Carroll FI, Partilla JS. 2001. Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse. 39:32-41.
80. Sara SJ. 2009. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci. 10:211-223.
81. Savasta M, Dubois A, Scatton B. 1986. Autoradiographic localization of D1 dopamine receptors in the rat brain with [3H]SCH 23390. Brain Res. 375:291-301.
82. Seamans JK, Gorelova N, Durstewitz D, Yang CR. 2001. Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci. 21:3628-3638.
83. Shankar H, Murugappan S, Kim S, Jin J, Ding Z, Wickman K, Kunapuli SP. 2004. Role of G protein-gated inwardly rectifying potassium channels in P2Y12 receptor-mediated platelet functional responses. Blood. 104:1335-1343.
84. Smith CC, Greene RW. 2012. CNS dopamine transmission mediated by noradrenergic innervation. J Neurosci. 32:6072-6080.
85. Sosulina L, Schwesig G, Seifert G, Pape HC. 2008. Neuropeptide Y activates a G-protein-coupled inwardly rectifying potassium current and dampens excitability in the lateral amygdala. Mol Cell Neurosci. 39:491-498.
86. Spencer SS, Spencer DD. 1994. Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia. 35:721-727.
87. Squire LR, Stark CE, Clark RE. 2004. The medial temporal lobe. Annu Rev Neurosci. 27:279-306.
88. Steffenach HA, Witter M, Moser MB, Moser EI. 2005. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron. 45:301-313.
89. Stenkamp K, Heinemann U, Schmitz D. 1998. Dopamine suppresses stimulus-induced field potentials in layer III of rat medial entorhinal cortex. Neurosci Lett. 255:119-121.
90. Steward O, Scoville SA. 1976. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol. 169:347-370.
91. Stuchlik A, Petrasek T, Vales K. 2008. Dopamine D2 receptors and alpha1-adrenoceptors synergistically modulate locomotion and behavior of rats in a place avoidance task. Behav Brain Res. 189:139-144.
92. Tarazi FI, Tomasini EC, Baldessarini RJ. 1999. Postnatal development of dopamine D1-like receptors in rat cortical and striatolimbic brain regions: an autoradiographic study. Dev Neurosci. 21:43-49.
93. Unnerstall JR, Fernandez I, Orensanz LM. 1985. The alpha-adrenergic receptor: radiohistochemical analysis of functional characteristics and biochemical differences. Pharmacol Biochem Behav. 22:859-874.
94. Unnerstall JR, Kopajtic TA, Kuhar MJ. 1984. Distribution of alpha 2 agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clonidine and related adrenergic agents. Brain Res. 319:69-101.
95. Varnai P, Osipenko ON, Vizi ES, Spat A. 1995. Activation of calcium current in voltage-clamped rat glomerulosa cells by potassium ions. J Physiol. 483(Pt 1):67-78.
96. Wadenberg ML, Hertel P, Fernholm R, Hygge Blakeman K, Ahlenius S, Svensson TH. 2000. Enhancement of antipsychotic-like effects by combined treatment with the alpha1-adrenoceptor antagonist prazosin and the dopamine D2 receptor antagonist raclopride in rats. J Neural Transm. 107:1229-1238.
97. Wang S, Chen X, Kurada L, Huang Z, Lei S. 2012. Activation of group II metabotropic glutamate receptors inhibits glutamatergic transmission in the rat entorhinal cortex via reduction of glutamate release probability. Cereb Cortex. 22:584-594.
98. Wang S, Zhang AP, Kurada L, Matsui T, Lei S. 2011. Cholecystokinin facilitates neuronal excitability in the entorhinal cortex via activation of TRPC-like channels. J Neurophysiol. 106:1515-1524.
99. Weiner DM, Levey AI, Sunahara RK, Niznik HB, O'Dowd BF, Seeman P, Brann MR. 1991. D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA. 88:1859-1863.
100. Wilcox BJ, Unnerstall JR. 1990. Identification of a subpopulation of neuropeptide Y-containing locus coeruleus neurons that project to the entorhinal cortex. Synapse. 6:284-291.
101. Witkowski G, Szulczyk B, Rola R, Szulczyk P. 2008. D (1) dopaminergic control of G protein-dependent inward rectifier K (+) (GIRK)-like channel current in pyramidal neurons of the medial prefrontal cortex. Neuroscience. 155:53-63.
102. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. 1989. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol. 33:161-253.
103. Witter MP, Naber PA, van Haeften T, Machielsen WC, Rombouts SA, Barkhof F, Scheltens P, Lopes da Silva FH. 2000. Corticohippocampal communication by way of parallel parahippocampalsubicular pathways. Hippocampus. 10:398-410.
104. Witter MP, Wouterlood FG, Naber PA, Van Haeften T. 2000. Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci. 911:1-24.
105. + channels. J Biol Chem. 284:10980-10991.
106. Xiao Z, Deng PY, Yang C, Lei S. 2009. Modulation of GABAergic transmission by muscarinic receptors in the entorhinal cortex of juvenile rats. J Neurophysiol. 102:659-669.
107. Zhang WP, Ouyang M, Thomas SA. 2004. Potency of catecholamines and other L-tyrosine derivatives at the cloned mouse adrenergic receptors. Neuropharmacology. 47:438-449.
108. Zhou FM, Hablitz JJ. 1999. Dopamine modulation of membrane and synaptic properties of interneurons in rat cerebral cortex. J Neurophysiol. 81:967-976.