Chronic treatment with anti-bipolar drugs causes intracellular alkalinization in astrocytes, altering their functions

Neurochemical Research

Volumn 37, Issue 11, 2012, Pages 2524-2540

  Song, Dan ^a   Li, Baoman ^a   Yan, Enzhi ^a   Man, Yi ^a   Wolfson, Marina ^b   Chen, Ye ^a   Peng, Liang ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Alkalinization; Arachidonic acid; Bipolar disorder; Ca2+ dependent phospholipase A2 (cPLA2); Fluorescence activated cell sorting (FACS); GluK2; Myo Inositol transporters

Indexed keywords

ARACHIDONIC ACID; CALCIUM ION; CARBAMAZEPINE; CPLA2 PROTEIN; GLUTAMATE RECEPTOR; GLUTAMINE; INOSITOL; INOSITOL PHOSPHATE; KAINIC ACID RECEPTOR; LITHIUM; PHOSPHOLIPASE A2; PHOSPHOLIPID; PROSTAGLANDIN; UNCLASSIFIED DRUG; VALPROIC ACID;

ALKALINIZATION; ARACHIDONIC ACID METABOLISM; ASTROCYTE; BIPOLAR DISORDER; BRAIN FUNCTION; BRAIN NERVE CELL; CELL CULTURE; CELL FUNCTION; CELL INTERACTION; CELL PH; HUMAN; MANIA; NERVOUS SYSTEM INFLAMMATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

ALKALIES; ANIMALS; ANTIPSYCHOTIC AGENTS; ASTROCYTES; BIPOLAR DISORDER; HYDROGEN-ION CONCENTRATION; LITHIUM COMPOUNDS; MICE;

ANIMALIA;

EID: 84871427792     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-012-0837-7     Document Type: Review

References (124)

1. Fankhauser MP, Benefield WH (1999) Bipolar disorder. In: Dipiro JT, Talbert RL, Yee GC et al (eds) Pharmacotherapy, 4th edn. McGraw-Hill, New York, pp 1161-1181
2. Kando JC, Wells BG, Hayes PE (1999) Depressive disorders. In: Dipiro JT, Talbert RL, Yee GC et al (eds) Pharmacotherapy, 4th edn. McGraw-Hill, New York, pp 1141-1160
3. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: Astrocytes process and control synaptic information. Trends Neurosci 32:421-431
4. Halassa MM, Haydon PG (2010) Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335-355
5. Machado-Vieira R, Manji HK, Zarate CA (2009) The role of the tripartite glutamatergic synapse in the pathophysiology and therapeutics of mood disorders. Neuroscientist 15:525-539
6. Hertz L (2011) Astrocytic energy metabolism and glutamate formation-relevance for 13C-NMR spectroscopy and importance of cytosolic/mitochondrial trafficking. Magn Reson Imag 29:1319-1329
7. Ongür D, Drevets WC, Price JL (1998) Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci USA 95:13290-13295
8. Rajkowska G (2000) Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol Psychiatry 48:766-777
9. Lubrich B, van Calker D (1999) Inhibition of the high affinity myo-inositol transport system: A common mechanism of action of antibipolar drugs? Neuropsychopharmacology 21:519-529
10. Wolfson M, Bersudsky Y, Zinger E et al (2000) Chronic treatment of human astrocytoma cells with lithium, carbamazepine or valproic acid decreases inositol uptake at high inositol concentrations but increases it at low inositol concentrations. Brain Res 855:158-161
11. Hertz L, Chen Y, Bersudsky Y et al (2004) Shared effects of all three conventional anti-bipolar drugs on the phosphoinositide system in astrocytes. In: Hertz L (ed) Non-neuronal cells of the nervous system: Function and dysfunction, 1st edn. Elsevier, Amsterdam, pp 1033-1048
12. Li B, Gu L, Zhang H et al (2007) Up-regulation of cPLA2 gene expression in astrocytes by all three conventional anti-bipolar drugs is drug-specific and enzyme-specific. Psychopharmacology 194:333-345
13. Li B, Zhang S, Li M et al (2009) Down-regulation of GluK2 kainate receptor expression by chronic treatment with moodstabilizing anti-convulsants or lithium in cultured astrocytes and brain, but not in neurons. Neuropharmacology 57:375-385
14. Song D, Du T, Li B et al (2008) Astrocytic alkalinization by therapeutically relevant lithium concentrations: Implications for myo-inositol depletion. Psychopharmacology 200:187-195
15. Williams RS, Cheng L, Mudge AW, Harwood AJ (2002) A common mechanism of action for three mood-stabilizing drugs. Nature 417:292-295
16. Di Daniel E, Cheng L, Maycox PR, Mudge AW(2006) The common inositol-reversible effect of mood stabilizers on neurons does not involve GSK3 inhibition, myo-inositol-1-phosphate synthase or the sodium-dependentmyo- inositol transporters.MolCellNeurosci 32:27-36
17. Shaltiel G, Dalton EC, Belmaker RH et al (2007) Specificity of mood stabilizer action on neuronal growth cones. Bipolar Disord 9:281-289
18. Owen DE, Egerton J (2012) Culture of dissociated sensory neurons from dorsal root ganglia of postnatal and adult rats. Methods Mol Biol 846:179-187
19. Scott BS (1977) Adult mouse dorsal root ganglia neurons in cell culture. J Neurobiol 8:417-427
20. Kim HJ, Thayer SA (2009) Lithium increases synapse formation between hippocampal neurons by depleting phosphoinositides. Mol Pharmacol 75:1021-1030
21. Persinger MA, Makarec K, Bradley JC (1988) Characteristics of limbic seizures evoked by peripheral injections of lithium and pilocarpine. Physiol Behav 44:27-37
22. Hertz L, Peng L, Lai JC (1998) Functional studies in cultured astrocytes. Methods 16:293-310
23. Hertz L (2012) Isotope-based quantitation of uptake, release, and metabolism of glutamate and glucose in cultured astrocytes. Methods Mol Biol 814:305-323
24. Barneda Ciurana D (2009) Estudi dels efectes del liti sobre el metabolisme dels fosfolipids i l'alliberació de senyals quimics en cultius d'astrocits (Lithium effects on phospholipids metabolism and signaling in cultured astrocytes). Ph. D. thesis, Universitat Autonoma de Barcelona, Spain
25. Lovatt D, Sonnewald U, Waagepetersen HS et al (2007) The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J Neurosci 27:12255-12266
26. Li B, Dong L, Wang B et al. (2012) Cell type-specific gene expression and editing responses to chronic fluoxetine treatment in the in vivo mouse brain and their relevance for stress-induced anhedonia. Neurochem Res. doi:10.1007/s11064-012-0814-1
27. Berridge MJ (1984) Inositol trisphosphate and diacylglycerol as second messengers. Biochem J 220:345-360
28. Fisher SK, Novak JE, Agranoff BW (2002) Inositol and higher inositol phosphates in neural tissues: Homeostasis, metabolism and functional significance. J Neurochem 82:736-754
29. 2+]i in cultured astrocytes by chronic treatment with a therapeutically relevant lithium concentration. Brain Res 711:245-248
30. 2+]i in astrocytes mimic those of acute inhibition of TRPC1 channel activity. Cell Calcium 50:42-53
31. Aukema HM, Holub BJ (1994) Inositol and pyrroloquinoline quinone. A: Inositol. In: Shils ME, Olson JA, Shike M (eds) Modern nutrition in health and disease, 8th edn. Lea and Febiger, Philadelphia, pp 466-473
32. Agam G, Shapiro Y, Bersudsky Y et al (1994) High dose peripheral inositol raises brain inositol levels and reverses behavioral effects of inositol depletion by lithium. Pharmacol Biochem Behav 49:341-343
33. Patishi Y, Lubrich B, Berger M et al (1996) Differential uptake of myo-inositol in vivo into rat brain areas. Eur Neuropsychopharmacol 6:73-75
34. Spector R, Lorenzo AV (1975) Myo-inositol transport in the central nervous system. Am J Physiol 228:1510-1518
35. Wong YH, Kalmbach SJ, Hartman BK, Sherman WR (1987) Immunohistochemical staining and enzyme activity measurements show myo-inositol-1-phosphate synthase to be localized in the vasculature of brain. J Neurochem 48:1434-1442
36. Forester BP, Finn CT, Berlow YA et al (2008) Brain lithium, N-acetyl aspartate and myo-inositol levels in older adults with bipolar disorder treated with lithium: A lithium-7 and proton magnetic resonance spectroscopy study. Bipolar Disord 10: 691-700
37. Silverstone PH, McGrath BM (2009) Lithium and valproate and their possible effects on the myo-inositol second messenger system in healthy volunteers and bipolar patients. Int Rev Psychiatry 21:414-423
38. Port JD, Unal SS, Mrazek DA, Marcus SM (2008) Metabolic alterations in medication-free patients with bipolar disorder: A 3T CSF-corrected magnetic resonance spectroscopic imaging study. Psychiatry Res 162:113-121
39. Wolfson M, Hertz E, Belmaker RH, Hertz L (1998) Chronic treatment with lithium and pretreatment with excess inositol reduce inositol pool size in astrocytes by different mechanisms. Brain Res 787:34-40
40. Matskevitch J, Wagner CA, Risler T et al (1998) Effect of extracellular pH on the myo-inositol transporter SMIT expressed in Xenopus oocytes. Pflugers Arch 436:854-857
41. Uldry M, Ibberson M, Horisberger JD et al (2001) Identification of a mammalian H?-myo-inositol symporter expressed predominantly in the brain. EMBO J 20:4467-4477
42. Fu H, Li B, Hertz L et al. (2012) Contributions in astrocytes of SMIT1/2 and HMIT to myo-inositol uptake at different concentrations and pH. Neurochem Int 61:187-194
43. McAlear SD, Bevensee MO (2004) pH regulation in non-neuronal brain cells and interstitial fluid. In: Hertz L (ed) Nonneuronal cells of the nervous system: Function and dysfunction, 1st edn. Elsevier, Amsterdam, pp 707-746
44. Pizzonia JH, Ransom BR, Pappas CA (1996) Characterization of Na+/H? exchange activity in cultured rat hippocampal astrocytes. J Neurosci Res 44:191-198
45. Aronson PS (1985) Properties of the renal Na+-H? exchanger. Ann NY Acad Sci 456:220-228
46. Janka Z, Szentistvanyi I, Juhasz A, Rimanoczy A (1980) Difference in lithium transport between neurones and glia in primary culture. Neuropharmacology 19:827-830
47. Hamakawa H, Murashita J, Yamada N et al (2004) Reduced intracellular pH in the basal ganglia and whole brain measured by 31P-MRS in bipolar disorder. Psychiatry Clin Neurosci 58:82-88
48. Di Daniel E, Mok MH, Mead E et al (2009) Evaluation of expression and function of the H?/myo-inositol transporter HMIT. BMC Cell Biol 10:54
49. Uldry M, Steiner P, Zurich MG et al (2004) Regulated exocytosis of an H?/myo-inositol symporter at synapses and growth cones. EMBO J 23:531-540
50. Di Daniel E, Kew JN, Maycox PR (2009) Investigation of the H?-myo-inositol transporter (HMIT) as a neuronal regulator of phosphoinositide signalling. Biochem Soc Trans 37:1139-1143
51. Gossman DG, Zhao HB (2008) Hemichannel-mediated inositol 1,4,5-trisphosphate (IP3) release in the cochlea: A novel mechanism of IP3 intercellular signaling. Cell Commun Adhes 15:305-315
52. Wang XH, Streeter M, Liu YP, Zhao HB (2009) Identification and characterization of pannexin expression in the mammalian cochlea. J Comp Neurol 512:336-346
53. 2+ waves guide CNS growth cones to remote regions of neuronal activity. PLoS One 3:e3692
54. 2+ acts as a mediator of communication from neurons to glia. Sci Signal 5:ra8
55. Zanotti S, Charles A (1997) Extracellular calcium sensing by glial cells: Low extracellular calcium induces intracellular calcium release and intercellular signaling. J Neurochem 69:594-602
56. Dowlatshahi D, MacQueen G, Wang JF et al (2000) Increased hippocampal supragranular Timm staining in subjects with bipolar disorder. NeuroReport 11:3775-3778
57. Ongür D, Jensen JE, Prescot AP et al (2008) Abnormal glutamatergic neurotransmission and neuronal-glial interactions in acute mania. Biol Psychiatry 64:718-726
58. Michael N, Erfurth A, Ohrmann P et al (2003) Acute mania is accompanied by elevated glutamate/glutamine levels within the left dorsolateral prefrontal cortex. Psychopharmacology 168:344-346
59. Connolly KR, Thase ME (2011) The clinical management of bipolar disorder: A review of evidence-based guidelines. Prim Care Companion CNS Disord 13 (pii:PCC.10r01097
60. Yoshizumi M, Eisenach JC, Hayashida K (2012) Riluzole and gabapentinoids activate glutamate transporters to facilitate glutamate-induced glutamate release from cultured astrocytes. Eur J Pharmacol 677:87-92
61. Brennan BP, Hudson JI, Jensen JE et al (2010) Rapid enhancement of glutamatergic neurotransmission in bipolar depression following treatment with riluzole. Neuropsychopharmacology 35:834-846
62. Zarate CA Jr, Brutsche NE, Ibrahim L et al (2012) Replication of Ketamine's antidepressant efficacy in bipolar depression: A randomized controlled add-on trial. Biol Psychiatry 71:939-946
63. Chowdhury GM, Behar KL, Cho W et al (2012) 1H-[13C]-nuclear magnetic resonance spectroscopy measures of ketamine's effect on amino acid neurotransmitter metabolism. Biol Psychiatry 71:1022-1025
64. Hansson E, Rönnbäck L (2004) Astrocytic resceptors and second messenger systems. In: Hertz L (ed) Non-neuronal cells of the nervous system: Function and dysfunction, 1st edn. Elsevier, Amsterdam, pp 475-501
65. Domingues AM, Taylor M, Fern R (2010) Glia as transmitter sources and sensors in health and disease. Neurochem Int 57:359-366
66. Jane DE, Lodge D, Collingridge GL (2009) Kainate receptors: Pharmacology, function and therapeutic potential. Neuropharmacology 56:90-113
67. Strutz-Seebohm N, Seebohm G, Shumilina E et al (2005) Glucocorticoid adrenal steroids and glucocorticoid-inducible kinase isoforms in the regulation of GluR6 expression. J Physiol 565:391-401
68. Brand-Schieber E, Lowery SL, Werner P (2004) Select ionotropic glutamate AMPA/kainate receptors are expressed at the astrocyte-vessel interface. Brain Res 1007:178-182
69. Cahoy JD, Emery B, Kaushal A et al (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 28:264-278
70. Beneyto M, Kristiansen LV, Oni-Orisan A et al (2007) Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 32:1888-1902
71. Benes FM, Lim B, Matzilevich D et al (2007) Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci USA 104:10164-10169
72. Schulze TG, Buervenich S, Badner JA et al (2005) Loci on chromosomes 6q and 6p interact to increase susceptibility to bipolar affective disorder in the national institute of mental health genetics initiative pedigrees. Biol Psychiatry 56:18-23
73. Parpura V, Zorec R (2010) Gliotransmission: Exocytotic release from astrocytes. Brain Res Rev 63:83-92
74. Yaguchi T, Nishizaki T (2010) Extracellular high K+ stimulates vesicular glutamate release from astrocytes by activating voltage-dependent calcium channels. J Cell Physiol 225:512-518
75. 2+ influx and extracellular signalregulated kinase phosphorylation in mouse astrocytes. J Psychiatry Neurosci 36:322-338
76. Bond DJ, Noronha MM, Kauer-Sant'Anna M et al (2008) Antidepressant- associated mood elevations in bipolar II disorder compared with bipolar I disorder and major depressive disorder: A systematic review and meta-analysis. J Clin Psychiatry 69:1589-1601
77. Kol S, Ruutiainen-Altman K, Ben-Shlomo I et al (1997) The rat ovarian phospholipase A2 system: Gene expression, cellular localization, activity characterization, and interleukin-1 dependence. Endocrinology 138:322-331
78. Purdon AD, Rosenberger TA, Shetty HU, Rapoport SI (2002) Energy consumption by phospholipid metabolism in mammalian brain. Neurochem Res 27:1641-1647
79. Lee HJ, Rao JS, Chang L et al (2008) Chronic N-methyl-Daspartate administration increases the turnover of arachidonic acid within brain phospholipids of the unanesthetized rat. J Lipid Res 49:162-168
80. Rapoport SI, Basselin M, Kim HW, Rao JS (2009) Bipolar disorder and mechanisms of action of mood stabilizers. Brain Res Rev 61:185-209
81. Basselin M, Fox MA, Chang L et al (2009) Imaging elevated brain arachidonic acid signaling in unanesthetized serotonin transporter (5-HTT)-deficient mice. Neuropsychopharmacology 34:1695-1709
82. Cussac D, Newman-Tancredi A, Quentric Y et al (2002) Characterization of phospholipase C activity at h5-HT2C compared with h5-HT2B receptors: Influence of novel ligands upon membrane-bound levels of [3H]phosphatidylinositols. Naunyn Schmiedebergs Arch Pharmacol 365:242-252
83. Brietzke E, Stertz L, Fernandes BS et al (2009) Comparison of cytokine levels in depressed, manic and euthymic patients with bipolar disorder. J Affect Disord 116:214-217
84. Hope S, Dieset I, Agartz I et al (2011) Affective symptoms are associated with markers of inflammation and immune activation in bipolar disorders but not in schizophrenia. J Psychiatr Res 45:1608-1616
85. Söderlund J, Olsson SK, Samuelsson M et al (2011) Elevation of cerebrospinal fluid interleukin-1 in bipolar disorder. J Psychiatry Neurosci 36:114-118
86. Rao JS, Harry GJ, Rapoport SI, Kim HW (2010) Increased excitotoxicity and neuroinflammatory markers in postmortem frontal cortex from bipolar disorder patients. Mol Psychiatry 15:384-392
87. Kim HW, Rapoport SI, Rao JS (2011) Altered arachidonic acid cascade enzymes in postmortem brain from bipolar disorder patients. Mol Psychiatry 16:419-428
88. Maida ME, Hurley SD, Daeschner JA et al (2006) Cytosolic prostaglandin E2 synthase (cPGES) expression is decreased in discrete cortical regions in psychiatric disease. Brain Res 1103:164-172
89. Weerasinghe GR, Rapoport SI, Bosetti F (2004) The effect of chronic lithium on arachidonic acid release and metabolism in rat brain does not involve secretory phospholipase A2 or lipoxygenase/cytochrome P450 pathways. Brain Res Bull 63: 485-489
90. Rao JS, Rapoport SI (2009) Mood-stabilizers target the brain arachidonic acid cascade. Curr Mol Pharmacol 2:207-214
91. Qu Y, Chang L, Klaff J et al (2006) Chronic fluoxetine upregulates arachidonic acid incorporation into the brain of unanesthetized rats. Eur Neuropsychopharmacol 16:561-571
92. Sun GY, Xu J, Jensen MD et al (2005) Phospholipase A2 in astrocytes: Responses to oxidative stress, inflammation, and G protein-coupled receptor agonists. Mol Neurobiol 31:27-41
93. Hewett SJ (1999) Interferon-gamma reduces cyclooxygenase-2-mediated prostaglandin E2 production from primary mouse astrocytes independent of nitric oxide formation. J Neuroimmunol 94:134-143
94. Font-Nieves M, Sans-Fons MG, Gorina R et al (2012) Induction of COX-2 enzyme and down-regulation of COX-1 expression by lipopolysaccharide (LPS) control prostaglandin E2 production in astrocytes. J Biol Chem 287:6454-6468
95. Xia M, Zhu Y (2011) Signaling pathways of ATP-induced PGE2 release in spinal cord astrocytes are EGFR transactivationdependent. Glia 59:664-674
96. Luo J, Lindström CL, Donahue A, Miller MW (2001) Differential effects of ethanol on the expression of cyclo-oxygenase in cultured cortical astrocytes and neurons. J Neurochem 76: 1354-1363
97. Nahman S, Belmaker RH, Azab AN (2012) Effects of lithium on lipopolysaccharide-induced inflammation in rat primary glia cells. Innate Immun 18:447-458
98. 2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia 50:91-106
99. 2+]i. NF-jB trafficking and transcription. PLoS One 3:e4093
100. Araque A (2008) Astrocytes process synaptic information. Neuron Glia Biol 4:3-10
101. Tharumaratnam D, Bashford S, Khan SA (2000) Indomethacin induced psychosis. Postgrad Med J 76:736-737
102. Clunie M, Crone LA, Klassen L, Yip R (2003) Psychiatric side effects of indomethacin in parturients. Can J Anaesth 50:586-588
103. Jiang HK, Chang DM (1999) Non-steroidal anti-inflammatory drugs with adverse psychiatric reactions: Five case reports. Clin Rheumatol 18:339-345
104. 2+ entry in cultured astrocytes. Biochem Biophys Res Commun 331:603-613
105. 2+ influx. Cell Calcium 33:283-292
106. Shuttleworth TJ (2012) STIM and Orai proteins and the noncapacitative ARC channels. Front Biosci 17:847-860
107. Yirmiya R, Goshen I (2011) Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25:181-213
108. O'Banion MK, Miller JC, Chang JW et al (1996) Interleukin-1b induces prostaglandin G/H synthase-2 (cyclooxygenase-2) in primary murine astrocyte cultures. J Neurochem 66:2532-2540
109. Song C, Phillips AG, Leonard B et al (2003) Interleukin 1b enhances conditioned fear memory in rats: Possible involvement of glucocorticoids. Eur J Neurosci 18:1739-1743
110. Ben Menachem-Zidon O, Avital A, Ben-Menahem Y et al (2011) Astrocytes support hippocampal-dependent memory and long-term potentiation via interleukin-1 signaling. Brain Behav Immun 25:1008-1016
111. Avital A, Goshen I, Kamsler A et al (2003) Impaired interleukin-1 signaling is associated with deficits in hippocampal memory processes and neural plasticity. Hippocampus 13:826-834
112. Goshen I, Kreisel T, Ounallah-Saad H et al (2007) A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrinology 32:1106-1115
113. Spulber S, Mateos L, Oprica M et al (2009) Impaired long term memory consolidation in transgenic mice overexpressing the human soluble form of IL-1ra in the brain. J Neuroimmunol 208:46-53
114. Besedovsky HO, del Rey A (2011) Central and peripheral cytokines mediate immune-brain connectivity. Neurochem Res 36:1-6
115. Bélanger M, Allaman I, Magistretti PJ (2011) Differential effects of pro-and anti-inflammatory cytokines alone or in combinations on the metabolic profile of astrocytes. J Neurochem 116:564-576
116. Ben Achour S, Pascual O (2010) Glia: The many ways to modulate synaptic plasticity. Neurochem Int 57:440-445
117. Beattie EC, Stellwagen D, Morishita W et al (2002) Control of synaptic strength by glial TNFa. Science 295:2282-2285
118. Stellwagen D, Malenka RC (2006) Synaptic scaling mediated by glial TNFa. Nature 440:1054-1059
119. Santello M, Bezzi P, Volterra A (2011) TNFa controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69:988-1001
120. Brennan FX, Beck KD, Servatius RJ (2004) Proinflammatory cytokines differentially affect leverpress avoidance acquisition in rats. Behav Brain Res 153:351-355
121. Brennan FX, Tieder JB 3rd (2006) Centrally administered tumor necrosis factor-a facilitates the avoidance performance of Sprague-Dawley rats. Brain Res 1109:142-145
122. Gibbs ME, Hutchinson D, Hertz L (2008) Astrocytic involvement in learning and memory consolidation. Neurosci Biobehav Rev 32:927-944
123. Hertz L, Gibbs ME (2009) What learning in day-old chickens can teach a neurochemist: Focus on astrocyte metabolism. J Neurochem 109(Suppl 1):10-16
124. Johnson FR, Ozdemir S, Manjunath R et al (2007) Factors that affect adherence to bipolar disorder treatments: A stated-preference approach. Med Care 45:545-552