Involvement of the nucleus accumbens shell dopaminergic system in prelimbic NMDA-induced anxiolytic-like behaviors

Neuropharmacology

Volumn 71, Issue , 2013, Pages 112-123

  Ahmadi, Hatam ^a   Nasehi, Mohammad ^b   Rostami, Parvin ^a   Zarrindast, Mohammad Reza ^c,d,e,f,g  

^a KHARAZMI UNIVERSITY   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c INSTITUTE FOR COGNITIVE SCIENCE STUDIES ICSS   (Iran)

^d TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^f TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^g INSTITUTE FOR RESEARCH IN FUNDAMENTAL SCIENCES IPM   (Iran)

Author keywords

Anxiety like behaviors; Dopaminergic system; Glutamatergic system; Nucleus accumbens shell; Prelimbic

Indexed keywords

CALCIUM CHANNEL; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; GLUTAMATERGIC SYSTEM; LIMBIC SYSTEM; MALE; MAZE TEST; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; DOPAMINERGIC NEURONS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; INJECTIONS, INTRAVENTRICULAR; MALE; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; NUCLEUS ACCUMBENS; PROTEIN ISOFORMS; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, DOPAMINE;

EID: 84878135019     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.03.017     Document Type: Article

References (112)

1. V. Bergink, H.J. van Megen, and H.G. Westenberg Glutamate and anxiety Eur. Neuropsychopharmacol. 14 2004 175 183
2. J.M. Boyce-Rustay, and A. Holmes Genetic inactivation of the NMDA receptor NR2A subunit has anxiolytic- and antidepressant-like effects in mice Neuropsychopharmacology 31 2006 2405 2414
3. A.M. Brady, and P. O'Donnell Dopaminergic modulation of prefrontal cortical input to nucleus accumbens neurons in vivo J. Neurosci. 24 2004 1040 1049
4. W.G. Brake, R.M. Sullivan, and A. Gratton Perinatal distress leads to lateralized medial prefrontal cortical dopamine hypofunction in adult rats J. Neurosci. 20 2000 5538 5543
5. L.H. Burns, T.W. Robbins, and B.J. Everitt Differential effects of excitotoxic lesions of the basolateral amygdala, ventral subiculum and medial prefrontal cortex on responding with conditioned reinforcement and locomotor activity potentiated by intra-accumbens infusions of D-amphetamine Behav. Brain Res. 55 1993 167 183
6. S. Cabib, E. Kempf, C. Schleef, A. Oliverio, and S. Puglisi-Allegra Effects of immobilization stress on dopamine and its metabolites in different brain areas of the mouse: role of genotype and stress duration Brain Res. 441 1988 153 160
7. J.N. Carlson, K.E. Visker, R.W. Keller Jr., and S.D. Glick Left and right 6-hydroxydopamine lesions of the medial prefrontal cortex differentially alter subcortical dopamine utilization and the behavioral response to stress Brain Res. 711 1996 1 9
8. A.P. Carobrez, and L.J. Bertoglio Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on Neurosci. Biobehav. Rev. 29 2005 1193 1205
9. B.M. Cortese, and K.L. Phan The role of glutamate in anxiety and related disorders CNS Spectr. 10 2005 820 830
10. I.C. da Cunha, A.P. Lopes, S.M. Steffens, A. Ferraz, J.C. Vargas, T.C. de Lima, J. Marino Neto, M.A. Paschoalini, and M.S. Faria The microinjection of AMPA receptor antagonist into the accumbens shell, but not into the accumbens core, induces anxiolysis in an animal model of anxiety Behav. Brain Res. 188 2008 91 99
11. H.N. David, K. Sissaoui, and J.H. Abraini Modulation of the locomotor responses induced by D1-like and D2-like dopamine receptor agonists and D-amphetamine by NMDA and non-NMDA glutamate receptor agonists and antagonists in the core of the rat nucleus accumbens Neuropharmacology 46 2004 179 191
12. R.J. Davidson, and W. Irwin The functional neuroanatomy of emotion and affective style Trends Cogn. Sci. 3 1999 11 21
13. M. Davis The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety Trends Pharmacol. Sci. 13 1992 35 41
14. M. Davis, W.A. Falls, S. Campeau, and M. Kim Fear-potentiated startle: a neural and pharmacological analysis Behav. Brain Res. 58 1993 175 198
15. A. Del Arco, and F. Mora Prefrontal cortex-nucleus accumbens interaction: in vivo modulation by dopamine and glutamate in the prefrontal cortex Pharmacol. Biochem. Behav. 90 2008 226 235
16. A. Del Arco, and F. Mora Neurotransmitters and prefrontal cortex-limbic system interactions: implications for plasticity and psychiatric disorders J. Neural Transm. 116 2009 941 952
17. A. Del Arco, G. Segovia, and F. Mora Blockade of NMDA receptors in the prefrontal cortex increases dopamine and acetylcholine release in the nucleus accumbens and motor activity Psychopharmacology (Berl) 201 2008 325 338
18. A.Y. Deutch, S.Y. Tam, and R.H. Roth Footshock and conditioned stress increase 3,4-dihydroxyphenylacetic acid (DOPAC) in the ventral tegmental area but not substantia nigra Brain Res. 333 1985 143 146
19. D.C. Ding, P.L. Gabbott, and S. Totterdell Differences in the laminar origin of projections from the medial prefrontal cortex to the nucleus accumbens shell and core regions in the rat Brain Res. 917 2001 81 89
20. M. Doherty, and A. Gratton Differential involvement of ventral tegmental GABA(A) and GABA(B) receptors in the regulation of the nucleus accumbens dopamine response to stress Brain Res. 1150 2007 62 68
21. A.J. Dunn Stress-related activation of cerebral dopaminergic systems Ann. N. Y. Acad. Sci. 537 1988 188 205
22. R.W. Dunn, R. Corbett, and S. Fielding Effects of 5-HT1A receptor agonists and NMDA receptor antagonists in the social interaction test and the elevated plus maze Eur. J. Pharmacol. 169 1989 1 10
23. M. Dziedzicka-Wasylewska, P. Willner, and M. Papp Changes in dopamine receptor mRNA expression following chronic mild stress and chronic antidepressant treatment Behav. Pharmacol. 8 1997 607 618
24. E.F. Espejo Selective dopamine depletion within the medial prefrontal cortex induces anxiogenic-like effects in rats placed on the elevated plus maze Brain Res. 762 1997 281 284
25. D. Forestiero, C.M. Manfrim, F.S. Guimaraes, and R.M. de Oliveira Anxiolytic-like effects induced by nitric oxide synthase inhibitors microinjected into the medial amygdala of rats Psychopharmacology (Berl) 184 2006 166 172
26. G.L. Forster, and C.D. Blaha Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area Eur. J. Neurosci. 12 2000 3596 3604
27. T.A. Fuller, F.T. Russchen, and J.L. Price Sources of presumptive glutamergic/aspartergic afferents to the rat ventral striatopallidal region J. Comp. Neurol. 258 1987 317 338
28. A.M. Garcia, R. Martinez, M.L. Brandao, and S. Morato Effects of apomorphine on rat behavior in the elevated plus-maze Physiol. Behav. 85 2005 440 447
29. P.A. Gargiulo Thyrotropin releasing hormone injected into the nucleus accumbens septi selectively increases face grooming in rats Braz. J. Med. Biol. Res. 29 1996 805 810
30. H. Garpenstrand, P. Annas, J. Ekblom, L. Oreland, and M. Fredrikson Human fear conditioning is related to dopaminergic and serotonergic biological markers Behav. Neurosci. 115 2001 358 364
31. A.A. Grace, S.B. Floresco, Y. Goto, and D.J. Lodge Regulation of firing of dopaminergic neurons and control of goal-directed behaviors Trends Neurosci. 30 2007 220 227
32. J.A. Gray Dopamine release in the nucleus accumbens: the perspective from aberrations of consciousness in schizophrenia Neuropsychologia 33 1995 1143 1153
33. Q. Greba, and L. Kokkinidis Peripheral and intraamygdalar administration of the dopamine D1 receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle Behav. Neurosci. 114 2000 262 272
34. H.J. Groenewegen, Y. Galis-de Graaf, and W.J. Smeets Integration and segregation of limbic cortico-striatal loops at the thalamic level: an experimental tracing study in rats J. Chem. Neuroanat. 16 1999 167 185
35. A. Hajizadeh Moghaddam, A. Roohbakhsh, P. Rostami, A. Heidary-Davishani, and M.R. Zarrindast GABA and histamine interaction in the basolateral amygdala of rats in the plus-maze test of anxiety-like behaviors Pharmacology 82 2008 59 66
36. M. Harte, and W.T. O'Connor Evidence for a selective prefrontal cortical GABA(B) receptor-mediated inhibition of glutamate release in the ventral tegmental area: a dual probe microdialysis study in the awake rat Neuroscience 130 2005 215 222
37. B.H. Harvey, and M. Shahid Metabotropic and ionotropic glutamate receptors as neurobiological targets in anxiety and stress-related disorders: focus on pharmacology and preclinical translational models Pharmacol. Biochem. Behav. 100 2012 775 800
38. L. Heimer, and G.F. Alheid Piecing together the puzzle of basal forebrain anatomy Adv. Exp. Med. Biol. 295 1991 1 42
39. A. Imperato, S. Puglisi-Allegra, A. Zocchi, M.G. Scrocco, P. Casolini, and L. Angelucci Stress activation of limbic and cortical dopamine release is prevented by ICS 205-930 but not by diazepam Eur. J. Pharmacol. 175 1990 211 214
40. T. Inoue, T. Izumi, Y. Maki, I. Muraki, and T. Koyama Effect of the dopamine D(1/5) antagonist SCH 23390 on the acquisition of conditioned fear Pharmacol. Biochem. Behav. 66 2000 573 578
41. T. Inoue, K. Tsuchiya, and T. Koyama Regional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain Pharmacol. Biochem. Behav. 49 1994 911 920
42. M.C. Jardim, D.C. Aguiar, F.A. Moreira, and F.S. Guimaraes Role of glutamate ionotropic and benzodiazepine receptors in the ventromedial hypothalamic nucleus on anxiety Pharmacol. Biochem. Behav. 82 2005 182 189
43. J.D. Jentsch, and R.H. Roth The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia Neuropsychopharmacology 20 1999 201 225
44. P.W. Kalivas, and P. Duffy Dopamine regulation of extracellular glutamate in the nucleus accumbens Brain Res. 761 1997 173 177
45. P.W. Kalivas, P. Duffy, and J. Barrow Regulation of the mesocorticolimbic dopamine system by glutamic acid receptor subtypes J. Pharmacol. Exp. Ther. 251 1989 378 387
46. A.E. Kelley, and L.C. Throne NMDA receptors mediate the behavioral effects of amphetamine infused into the nucleus accumbens Brain Res. Bull. 29 1992 247 254
47. P. Kostopoulos, and M. Petrides Left mid-ventrolateral prefrontal cortex: underlying principles of function Eur. J. Neurosci. 27 2008 1037 1049
48. A. Louilot, M. Le Moal, and H. Simon Differential reactivity of dopaminergic neurons in the nucleus accumbens in response to different behavioral situations. An in vivo voltammetric study in free moving rats Brain Res. 397 1986 395 400
49. G. Martinez, C. Ropero, A. Funes, E. Flores, C. Blotta, A.I. Landa, and P.A. Gargiulo Effects of selective NMDA and non-NMDA blockade in the nucleus accumbens on the plus-maze test Physiol. Behav. 76 2002 219 224
50. R.J. Mathew, B.T. Ho, D.L. Taylor, and K.M. Semchuk Catecholamine and dopamine-beta-hydroxylase in anxiety J. Psychosom Res. 25 1981 499 504
51. A. Meyer-Lindenberg, R.S. Miletich, P.D. Kohn, G. Esposito, R.E. Carson, M. Quarantelli, D.R. Weinberger, and K.F. Berman Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia Nat. Neurosci. 5 2002 267 271
52. M.L. Molchanov, and F.S. Guimaraes Anxiolytic-like effects of AP7 injected into the dorsolateral or ventrolateral columns of the periaqueductal gray of rats Psychopharmacology (Berl) 160 2002 30 38
53. M.F. Montaron, J.M. Deniau, A. Menetrey, J. Glowinski, and A.M. Thierry Prefrontal cortex inputs of the nucleus accumbens-nigro-thalamic circuit Neuroscience 71 1996 371 382
54. F. Mora, and M. Cobo The neurobiological basis of prefrontal cortex self-stimulation: a review and an integrative hypothesis Prog. Brain Res. 85 1990 419 431
55. M. Morari, M. Marti, S. Sbrenna, K. Fuxe, C. Bianchi, and L. Beani Reciprocal dopamine-glutamate modulation of release in the basal ganglia Neurochem. Int. 33 1998 383 397
56. T. Motevasseli, A. Rezayof, M.R. Zarrindast, and T. Nayer-Nouri Role of ventral hippocampal NMDA receptors in anxiolytic-like effect of morphine Physiol. Behav. 101 2010 608 613
57. S. Murase, J. Grenhoff, G. Chouvet, F.G. Gonon, and T.H. Svensson Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studied in vivo Neurosci. Lett. 157 1993 53 56
58. L.P. Nascimento Hackl, and A.P. Carobrez Distinct ventral and dorsal hippocampus AP5 anxiolytic effects revealed in the elevated plus-maze task in rats Neurobiol. Learn. Mem. 88 2007 177 185
59. M. Nasehi, F. Mafi, S. Oryan, S. Nasri, and M.R. Zarrindast The effects of dopaminergic drugs in the dorsal hippocampus of mice in the nicotine-induced anxiogenic-like response Pharmacol. Biochem. Behav. 98 2011 468 473
60. M. Nasehi, M. Piri, N. Jamali-Raeufy, and M.R. Zarrindast Influence of intracerebral administration of NO agents in dorsal hippocampus (CA1) on cannabinoid state-dependent memory in the step-down passive avoidance test Physiol. Behav. 100 2010 297 304
61. J.F. Navarro, G. Luna, F. Garcia, and C. Pedraza Effects of L-741,741, a selective dopamine receptor antagonist, on anxiety tested in the elevated plus-maze in mice Methods Find Exp. Clin. Pharmacol. 25 2003 45 47
62. D. Ongur, and J.L. Price The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans Cereb. Cortex 10 2000 206 219
63. C.M. Padovan, and F.S. Guimaraes Restraint-induced hypoactivity in an elevated plus-maze Braz. J. Med. Biol. Res. 33 2000 79 83
64. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates sixth ed. 2007 Academic Press London. UK
65. S. Pellow, P. Chopin, S.E. File, and M. Briley Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J. Neurosci. Methods 14 1985 149 167
66. M. Perez de la Mora, A. Gallegos-Cari, M. Crespo-Ramirez, D. Marcellino, A.C. Hansson, and K. Fuxe Distribution of dopamine D(2)-like receptors in the rat amygdala and their role in the modulation of unconditioned fear and anxiety Neuroscience 201 2012 252 266
67. M.A. Pezze, and J. Feldon Mesolimbic dopaminergic pathways in fear conditioning Prog. Neurobiol. 74 2004 301 320
68. A. Plaznik, W. Palejko, M. Nazar, and M. Jessa Effects of antagonists at the NMDA receptor complex in two models of anxiety Eur. Neuropsychopharmacol. 4 1994 503 512
69. S. Puglisi-Allegra, A. Imperato, L. Angelucci, and S. Cabib Acute stress induces time-dependent responses in dopamine mesolimbic system Brain Res. 554 1991 217 222
70. J.F. Reinhard Jr., M.J. Bannon, and R.H. Roth Acceleration by stress of dopamine synthesis and metabolism in prefrontal cortex: antagonism by diazepam Naunyn Schmiedebergs Arch. Pharmacol. 318 1982 374 377
71. F.L. Reis, S. Masson, A.R. de Oliveira, and M.L. Brandao Dopaminergic mechanisms in the conditioned and unconditioned fear as assessed by the two-way avoidance and light switch-off tests Pharmacol. Biochem. Behav. 79 2004 359 365
72. C. Riaza Bermudo-Soriano, M.M. Perez-Rodriguez, C. Vaquero-Lorenzo, and E. Baca-Garcia New perspectives in glutamate and anxiety Pharmacol. Biochem. Behav. 100 2012 752 774
73. T.W. Robbins From arousal to cognition: the integrative position of the prefrontal cortex Prog. Brain Res. 126 2000 469 483
74. T.W. Robbins, and B.J. Everitt Neurobehavioural mechanisms of reward and motivation Curr. Opin. Neurobiol. 6 1996 228 236
75. H.M. Robinson, S.D. Hood, C.J. Bell, and D.J. Nutt Dopamine and social anxiety disorder Rev. Bras Psiquiatr. 28 2006 263 264
76. R.J. Rodgers, E.M. Nikulina, and J.C. Cole Dopamine D1 and D2 receptor ligands modulate the behaviour of mice in the elevated plus-maze Pharmacol. Biochem. Behav. 49 1994 985 995
77. M.A. Rogers, K. Kasai, M. Koji, R. Fukuda, A. Iwanami, K. Nakagome, M. Fukuda, and N. Kato Executive and prefrontal dysfunction in unipolar depression: a review of neuropsychological and imaging evidence Neurosci. Res. 50 2004 1 11
78. P. Rostami, A. Hajizadeh-Moghaddam, and M.R. Zarrindast The effects of histaminergic agents in the ventral hippocampus of rats in the plus-maze test of anxiety-like behaviours Physiol. Behav. 87 2006 891 896
79. J.D. Salamone, M.S. Cousins, and B.J. Snyder Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis Neurosci. Biobehav. Rev. 21 1997 341 359
80. F. Sargolini, P. Roullet, A. Oliverio, and A. Mele Effects of lesions to the glutamatergic afferents to the nucleus accumbens in the modulation of reactivity to spatial and non-spatial novelty in mice Neuroscience 93 1999 855 867
81. S.C. Sealfon, and C.W. Olanow Dopamine receptors: from structure to behavior Trends Neurosci. 23 2000 S34 S40
82. S.R. Sesack, and V.M. Pickel Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area J. Comp. Neurol. 320 1992 145 160
83. A.A. Shah, T. Sjovold, and D. Treit Selective antagonism of medial prefrontal cortex D4 receptors decreases fear-related behaviour in rats Eur. J. Neurosci. 19 2004 3393 3397
84. Y. Shirayama, and S. Chaki Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents Curr. Neuropharmacol 4 2006 277 291
85. A.B. Simon, and J.M. Gorman Advances in the treatment of anxiety: targeting glutamate NeuroRx 3 2006 57 68
86. P. Somogyi, G. Tamas, R. Lujan, and E.H. Buhl Salient features of synaptic organisation in the cerebral cortex Brain Res. Brain Res. Rev. 26 1998 113 135
87. C.A. Stern, F.H. Do Monte, L. Gazarini, A.P. Carobrez, and L.J. Bertoglio Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest Neuroscience 170 2010 214 222
88. C.W. Stevenson, R.M. Sullivan, and A. Gratton Effects of basolateral amygdala dopamine depletion on the nucleus accumbens and medial prefrontal cortical dopamine responses to stress Neuroscience 116 2003 285 293
89. R.M. Sullivan, and H. Szechtman Asymmetrical influence of mesocortical dopamine depletion on stress ulcer development and subcortical dopamine systems in rats: implications for psychopathology Neuroscience 65 1995 757 766
90. M.T. Taber, and H.C. Fibiger Electrical stimulation of the prefrontal cortex increases dopamine release in the nucleus accumbens of the rat: modulation by metabotropic glutamate receptors J. Neurosci. 15 1995 3896 3904
91. R. Takahata, and B. Moghaddam Activation of glutamate neurotransmission in the prefrontal cortex sustains the motoric and dopaminergic effects of phencyclidine Neuropsychopharmacology 28 2003 1117 1124
92. A.N. Talalaenko, I.A. Abramets, V. Stakhovskii Yu, A.A. Shekhovtsov, A.V. Chernikov, and S.L. Shevchenko The role of dopaminergic mechanisms on the brain in various models of anxious states Neurosci. Behav. Physiol. 24 1994 284 288
93. C. Timothy, B. Costall, and J.W. Smythe Effects of SCH23390 and raclopride on anxiety-like behavior in rats tested in the black-white box Pharmacol. Biochem. Behav. 62 1999 323 327
94. H.B. Uylings, H.J. Groenewegen, and B. Kolb Do rats have a prefrontal cortex? Behav. Brain Res. 146 2003 3 17
95. A.A. Walf, and C.A. Frye The use of the elevated plus maze as an assay of anxiety-related behavior in rodents Nat. Protoc. 2 2007 322 328
96. P.M. Wall, R.J. Blanchard, M. Yang, and D.C. Blanchard Infralimbic D2 receptor influences on anxiety-like behavior and active memory/attention in CD-1 mice Prog. Neuropsychopharmacol. Biol. Psychiatry 27 2003 395 410
97. W. Wang, D. Dever, J. Lowe, G.P. Storey, A. Bhansali, E.K. Eck, I. Nitulescu, J. Weimer, and N.S. Bamford Regulation of prefrontal excitatory neurotransmission by dopamine in the nucleus accumbens core J. Physiol. 590 2012 3743 3769
98. J.M. Wieronska, B. Szewczyk, A. Palucha, P. Branski, and M. Smialowska Involvement of CRF but not NPY in the anxiety regulation via NMDA receptors Pol. J. Pharmacol. 55 2003 1119 1124
99. M. Wu, S.M. Brudzynski, and G.J. Mogenson Functional interaction of dopamine and glutamate in the nucleus accumbens in the regulation of locomotion Can. J. Physiol. Pharmacol. 71 1993 407 413
100. T. Yamaguchi, H.L. Wang, X. Li, T.H. Ng, and M. Morales Mesocorticolimbic glutamatergic pathway J. Neurosci. 31 2011 8476 8490
101. D.S. Zahm, and J.S. Brog On the significance of subterritories in the "accumbens" part of the rat ventral striatum Neuroscience 50 1992 751 767
102. M.R. Zarrindast, A. Aghamohammadi-Sereshki, A. Rezayof, and P. Rostami Nicotine-induced anxiogenic-like behaviours of rats in the elevated plus-maze: possible role of NMDA receptors of the central amygdala J. Psychopharmacol. 26 2012 555 563
103. M.R. Zarrindast, S. Babapoor-Farrokhran, and A. Rezayof Involvement of opioidergic system of the ventral hippocampus, the nucleus accumbens or the central amygdala in anxiety-related behavior Life Sci. 82 2008 1175 1181
104. M.R. Zarrindast, S. Mahboobi, M.S. Sadat-Shirazi, and S. Ahmadi Anxiolytic-like effect induced by the cannabinoid CB1 receptor agonist, arachydonilcyclopropylamide (ACPA), in the rat amygdala is mediated through the D1 and D2 dopaminergic systems J. Psychopharmacol. 25 2011 131 140
105. M.R. Zarrindast, A.H. Moghadam, P. Rostami, and A. Roohbakhsh The effects of histaminergic agents in the central amygdala of rats in the elevated plus-maze test of anxiety Behav. Pharmacol. 16 2005 643 649
106. M.R. Zarrindast, M. Nasehi, M. Khansari, and M. Bananej Influence of nitric oxide agents in the rat amygdala on anxiogenic-like effect induced by histamine Neurosci. Lett. 489 2011 38 42
107. M.R. Zarrindast, M. Nasehi, M. Piri, and P. Bina Anxiety-like behavior induced by histaminergic agents can be prevented by cannabinoidergic WIN55,212-2 injected into the dorsal hippocampus in mice Pharmacol. Biochem. Behav. 94 2010 387 396
108. M.R. Zarrindast, M. Nasehi, M. Piri, and N. Heidari Effects of cholinergic system of dorsal hippocampus of rats on MK-801 induced anxiolytic-like behavior Neurosci. Lett. 505 2011 65 70
109. M.R. Zarrindast, J. Solati, S. Oryan, and K. Parivar Effect of intra-amygdala injection of nicotine and GABA receptor agents on anxiety-like behaviour in rats Pharmacology 82 2008 276 284
110. M.R. Zarrindast, M. Torabi, P. Rostami, and S. Fazli-Tabaei The effects of histaminergic agents in the dorsal hippocampus of rats in the elevated plus-maze test of anxiety Pharmacol. Biochem. Behav. 85 2006 500 506
111. M.R. Zarrindast, F. Valizadegan, P. Rostami, and A. Rezayof Histaminergic system of the lateral septum in the modulation of anxiety-like behaviour in rats Eur. J. Pharmacol. 583 2008 108 114
112. F.M. Zhou, and J.J. Hablitz Dopamine modulation of membrane and synaptic properties of interneurons in rat cerebral cortex J. Neurophysiol. 81 1999 967 976