Involvement of the dopamine receptors in the basolateral amygdala (BLA) in the effects of histamine on anxiety-like behaviors of the elevated plus maze in male Wistar rats was investigated. The results showed that bilateral intra-BLA injections of histamine (2.5, 5 and 7.5 µg/rat) induced an anxiogenic-like effect, revealed by decreases in percentage of open arm time (%OAT) and open arm entries (%OAE). Intra-BLA administration of dopamine D1 receptor agonist, SKF38393 (0.25 µg/rat), and dopamine D2 receptor agonist, quinpirole (0.03 and 0.05 µg/rat), decreased %OAT but not %OAE. Conversely, intra-BLA administration of dopamine D1 receptor antagonist, SCH23390 (0.5 and 1 µg/rat), and dopamine D2 receptor antagonist, sulpiride (0.3 and 0.5 µg/rat), increased %OAT and %OAE, suggesting an anxiolytic-like effect for both drugs. Interestingly, co-administration of a silent dose of SCH23390 or sulpiride prevented anxiogenic-like effects of SKF38393 and quinpirole, respectively. Conjoint administration of a sub-effective dose of SKF38393 (0.125 µg/rat) or quinpirole (0.01 µg/rat) along with lower doses of histamine (1 and 2.5 µg/rat) induced anxiolytic-like effects. On the other hand, intra-BLA pretreatment with a silent dose of SCH23390 (0.25 µg/rat) or sulpiride (0.1 µg/rat) prevented the anxiogenic-like effect of higher doses of histamine (5 and 7.5 µg/rat). No significant change was observed in total closed arm entries, as an index for motor activity of the animals. It can be concluded that the dopamine D1 and D2 receptors in the BLA may be involved in the anxiogenic-like effects induced by histamine.
AmaralDGCorbettBA (2003) The amygdala, autism and anxiety. Novartis Found Symp251: 177–187.
2.
BartoszykGD (1998) Anxiolytic effects of dopamine receptor ligands: I. Involvement of dopamine autoreceptors. Life Sci62: 649–663.
3.
BrandaoMLAnseloniVZPandossioJE. (1999) Neurochemical mechanisms of the defensive behavior in the dorsal midbrain. Neurosci Biobehav Rev23: 863–875.
4.
BrownREStevensDRHaasHL (2001) The physiology of brain histamine. Prog Neurobiol63: 637–672.
5.
BuenoCHZangrossiHJrVianaMB (2005) The inactivation of the basolateral nucleus of the rat amygdala has an anxiolytic effect in the elevated T-maze and light/dark transition tests. Braz J Med Biol Res38: 1697–1701.
6.
CocoMLKuhnCMElyTD. (1992) Selective activation of mesoamygdaloid dopamine neurons by conditioned stress: attenuation by diazepam. Brain Res590: 39–47.
7.
DavisMRainnieDCassellM (1994) Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci17: 208–214.
8.
de la MoraMPCardenas-CachonLVazquez-GarciaM. (2005) Anxiolytic effects of intra-amygdaloid injection of the D1 antagonist SCH23390 in the rat. Neurosci Lett377: 101–105.
9.
de OliveiraARReimerAEBrandaoML (2006) Dopamine D2 receptor mechanisms in the expression of conditioned fear. Pharmacol Biochem Behav84: 102–111.
10.
de OliveiraARReimerAEBrandaoML (2009) Role of dopamine receptors in the ventral tegmental area in conditioned fear. Behav Brain Res199: 271–277.
11.
GrebaQGifkinsAKokkinidisL (2001) Inhibition of amygdaloid dopamine D2 receptors impairs emotional learning measured with fear-potentiated startle. Brain Res899: 218–226.
12.
HaasHPanulaP (2003) The role of histamine and the tuberomamillary nucleus in the nervous system. Nat Rev Neurosci4: 121–130.
13.
HaasHLSergeevaOASelbachO (2008) Histamine in the nervous system. Physiol Rev88: 1183–1241.
14.
Hajizadeh MoghaddamARoohbakhshARostamiP. (2008) GABA and histamine interaction in the basolateral amygdala of rats in the plus-maze test of anxiety-like behaviors. Pharmacology82: 59–66.
15.
HombergJRvan den AkkerMRaasoHS. (2002) Enhanced motivation to self-administer cocaine is predicted by self-grooming behaviour and relates to dopamine release in the rat medial prefrontal cortex and amygdala. Eur J Neurosci15: 1542–1550.
16.
HuangCCHsuKSGeanPW (1996) Isoproterenol potentiates synaptic transmission primarily by enhancing presynaptic calcium influx via P- and/or Q-type calcium channels in the rat amygdala. J Neurosci16: 1026–1033.
17.
InglisFMMoghaddamB (1999) Dopaminergic innervation of the amygdala is highly responsive to stress. J Neurochem72: 1088–1094.
18.
InoueTIzumiTLiXB. (2005) Effect of a dopamine D1/5 receptor antagonist on haloperidol-induced inhibition of the acquisition of conditioned fear. Eur J Pharmacol519: 253–258.
19.
ItoCShenHToyotaH. (1999) Effects of the acute and chronic restraint stresses on the central histaminergic neuron system of Fischer rat. Neurosci Lett262: 143–145.
20.
LeDouxJE (2000) Emotion circuits in the brain. Annu Rev Neurosci23: 155–184.
21.
Malmberg-AielloPIpponiABartoliniA. (2002) Mouse light/dark box test reveals anxiogenic-like effects by activation of histamine H1 receptors. Pharmacol Biochem Behav71: 313–318.
22.
MillanMJ (2003) The neurobiology and control of anxious states. Prog Neurobiol70: 83–244.
23.
PanulaPPirvolaUAuvinenS. (1989) Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience28: 585–610.
24.
ParkKYiJHKimH. (2011) HCN channel activity-dependent modulation of inhibitory synaptic transmission in the rat basolateral amygdala. Biochem Biophys Res Commun404: 952–957.
25.
PassaniMBGiannoniPBucherelliC. (2007) Histamine in the brain: beyond sleep and memory. Biochem Pharmacol73: 1113–1122.
26.
PaxinosGWatsonC (2007) The rat brain in stereotaxic coordinates, 6th edition. Amsterdam: Academic Press.
27.
PhelpsEALeDouxJE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron48: 175–187.
28.
PonnusamyRNissimHABaradM (2005) Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. Learn Mem12: 399–406.
29.
PrivouCKnocheAHasenohrlRU. (1998) The H1- and H2-histamine blockers chlorpheniramine and ranitidine applied to the nucleus basalis magnocellularis region modulate anxiety and reinforcement related processes. Neuropharmacology37: 1019–1032.
30.
RezayofAHosseiniSSZarrindastMR (2009) Effects of morphine on rat behaviour in the elevated plus maze: the role of central amygdala dopamine receptors. Behav Brain Res202: 171–178.
31.
RodgersRJJohnsonNJ (1995) Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol Biochem Behav52: 297–303.
32.
RodgersRJNikulinaEMColeJC (1994) Dopamine D1 and D2 receptor ligands modulate the behaviour of mice in the elevated plus-maze. Pharmacol Biochem Behav49: 985–995.
33.
SahPFaberESLopez De ArmentiaM. (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev83: 803–834.
34.
Saldivar-GonzalezJAPosadas-AndrewsARodriguezR. (2003) Effect of electrical stimulation of the baso-lateral amygdala nucleus on defensive burying shock probe test and elevated plus maze in rats. Life Sci72: 819–829.
35.
SuzukiTIshigookaJWatanabeS. (2002) Enhancement of delayed release of dopamine in the amygdala induced by conditioned fear stress in methamphetamine-sensitized rats. Eur J Pharmacol435: 59–65.
36.
SwansonLW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull9: 321–353.
37.
SwansonLWPetrovichGD (1998) What is the amygdala?. Trends Neurosci21: 323–331.
38.
TaylorKMSnyderSH (1971) Brain histamine: rapid apparent turnover altered by restraint and cold stress. Science172: 1037–1039.
39.
ThielCMSchwartingRK (2001) Dopaminergic lateralisation in the forebrain: relations to behavioural asymmetries and anxiety in male Wistar rats. Neuropsychobiology43: 192–199.
40.
TimmJMarrIWerthweinS. (1998) H2 receptor-mediated facilitation and H3 receptor-mediated inhibition of noradrenaline release in the guinea-pig brain. Naunyn Schmiedebergs Arch Pharmacol357: 232–239.
41.
TimothyCCostallBSmytheJW (1999) Effects of SCH23390 and raclopride on anxiety-like behavior in rats tested in the black-white box. Pharmacol Biochem Behav62: 323–327.
42.
TzavaraETWadeMNomikosGG (2003) Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J Neurosci23: 9374–9384.
ZahmDSTrimbleM (2008) The dopaminergic projection system, basal forebrain macrosystems, and conditioned stimuli. CNS Spectr13: 32–40.
45.
ZarrindastMRKhodarahmiPRezayofA. (2010a) Withdrawal from repeated administration of morphine alters histamine-induced anxiogenic effects produced by intra-ventral hippocampal microinjection. J Psychopharmacol24: 881–889.
46.
ZarrindastMRMoghadamAHRostamiP. (2005a) The effects of histaminergic agents in the central amygdala of rats in the elevated plus-maze test of anxiety. Behav Pharmacol16: 643–649.
47.
ZarrindastMRNaghdi-SedehNNasehiM. (2010b) The effects of dopaminergic drugs in the ventral hippocampus of rats in the nicotine-induced anxiogenic-like response. Neurosci Lett475: 156–160.
48.
ZarrindastMRNasehiMRostamiP. (2005b) Repeated administration of dopaminergic agents in the dorsal hippocampus and morphine-induced place preference. Behav Pharmacol16: 85–92.
49.
ZarrindastMRRezayofASahraeiH. (2003) Involvement of dopamine D1 receptors of the central amygdala on the acquisition and expression of morphine-induced place preference in rat. Brain Res965: 212–221.
50.
ZarrindastMRRostamiPZareiM. (2005c) Intracerebroventricular effects of histaminergic agents on morphine-induced anxiolysis in the elevated plus-maze in rats. Basic Clin Pharmacol Toxicol97: 276–281.
51.
ZarrindastMRSarahroodiSArziA. (2008a) Cannabinoid CB1 receptors of the rat central amygdala mediate anxiety-like behaviour: interaction with the opioid system. Behav Pharmacol19: 716–723.
52.
ZarrindastMRTorabiMRostamiP. (2006) The effects of histaminergic agents in the dorsal hippocampus of rats in the elevated plus-maze test of anxiety. Pharmacol Biochem Behav85: 500–506.
53.
ZarrindastMRValizadeganFRostamiP. (2008b) Histaminergic system of the lateral septum in the modulation of anxiety-like behaviour in rats. Eur J Pharmacol583: 108–114.
