Functional correlation between GABAergic and dopaminergic systems of dorsal hippocampus and ventral tegmental area in passive avoidance learning in rats

Neuroscience

Volumn 196, Issue , 2011, Pages 104-114

  Nazari Serenjeh, F ^a   Rezayof, A ^a   Zarrindast, M R ^b,c  

^a UNIVERSITY OF TEHRAN   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

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

Author keywords

Hippocampus; Muscimol; Rat(s); SCH23390; Sulpiride; Ventral tegmental area

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR; MUSCIMOL; SULPIRIDE;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANNULA; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; MALE; MEMORY; MEMORY DISORDER; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; RAT; STEREOTACTIC PROCEDURE; TASK PERFORMANCE; TRAINING; VENTRAL TEGMENTUM; WISTAR RAT;

AMNESIA; ANIMALS; AVOIDANCE LEARNING; BENZAZEPINES; DOPAMINE ANTAGONISTS; DOPAMINERGIC NEURONS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; GABA-A RECEPTOR AGONISTS; GABAERGIC NEURONS; HIPPOCAMPUS; MALE; MENTAL RECALL; MICROINJECTIONS; MUSCIMOL; RATS; RATS, WISTAR; SULPIRIDE; VENTRAL TEGMENTAL AREA;

EID: 80054044947     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.08.073     Document Type: Article

References (73)

1. Adell A., Artigas F. The somatodendritic release of dopamine in the ventral tegmental area and its regulation by afferent transmitter systems. Neurosci Biobehav Rev 2004, 28:415-431.
2. Bethus I., Tse D., Morris R.G. Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 2010, 30:1610-1618.
3. Bettler B., Kaupmann K., Mosbacher J., Gassmann M. Molecular structure and physiological functions of GABA(B) receptors. Physiol Rev 2004, 84:835-867.
4. Bozzi Y., Vallone D., Borrelli E. Neuroprotective role of dopamine against hippocampal cell death. J Neurosci 2000, 20:8643-8649.
5. Brinschwitz K., Dittgen A., Madai V.I., Lommel R., Geisler S., Veh R.W. Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 2010, 168:463-476.
6. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002, 35:625-641.
7. Cameron D.L., Williams J.T. Dopamine D1 receptors facilitate transmitter release. Nature 1993, 366:344-347.
8. Carr D.B., Sesack S.R. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 2000, 20. 3964-3873.
9. Carr D.B., Sesack S.R. GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 2000, 38:114-123.
10. Chebib M., Johnston G.A. GABA-activated ligand gated ion channels: medicinal chemistry and molecular biology. J Med Chem 2000, 43:1427-1447.
11. Chen N.N., Pan W.H. Regulatory effects of D2 receptors in the ventral tegmental area on the mesocorticolimbic dopaminergic pathway. J Neurochem 2000, 74:2576-2582.
12. De Lima M.N., Luft T., Roesler R., Schröder N. Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory. Neurosci Lett 2006, 405:142-146.
13. De Oliveira A.R., Reimer A.E., Brandão M.L. Role of dopamine receptors in the ventral tegmental area in conditioned fear. Behav Brain Res 2009, 199:271-277.
14. Ding Z.M., Liu W., Engleman E.A., Rodd Z.A., McBride W.J. Differential effects of dopamine D2 and GABA(A) receptor antagonists on dopamine neurons between the anterior and posterior ventral tegmental area of female Wistar rats. Pharmacol Biochem Behav 2009, 92:404-412.
15. El-Ghundi M., O'Dowd B.F., George S.R. Insights into the role of dopamine receptor systems in learning and memory. Rev Neurosci 2007, 8:37-66.
16. Farr S.A., Flood J.F., Morley J.E. The effect of cholinergic, GABAergic, serotonergic, and glutamatergic receptor modulation on posttrial memory processing in the hippocampus. Neurobiol Learn Mem 2000, 73:150-167.
17. Floresco S.B., Todd C.L., Grace A.A. Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J Neurosci 2001, 21:4915-4922.
18. Frey U., Schroeder H., Matthies H. Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices. Brain Res 1990, 522:69-75.
19. Gasbarri A., Sulli A., Innocenzi R., Pacitti C., Brioni J.D. Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat. Neuroscience 1996, 74:1037-1044.
20. Gasbarri A., Sulli A., Packard M.G. The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 1997, 21:1-22.
21. Gavello-Baudy S., Le Merrer J., Decortel L., David V., Cazala P. Self-administration of the GABAA agonist muscimol into the medial septum: dependence on dopaminergic mechanisms. Psychopharmacology (Berl) 2008, 201:219-228.
22. Goto Y., Grace A.A. Dopamine modulation of hippocampal-prefrontal cortical interaction drives memory-guided behavior. Cereb Cortex 2008, 18:1407-1414.
23. Goto Y., Yang C.R., Otani S. Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders. Biol Psychiatry 2010, 67:199-207.
24. Gurden H., Tassin J.P., Jay T.M. Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation. Neuroscience 1999, 94:1019-1027.
25. Izquierdo I., Medina J.H. Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol Learn Mem 1995, 63:19-32.
26. Jaber M., Robinson S.W., Missale C., Carron M.G. Dopamine receptors and brain function. Neuropharmacology 1996, 35:1503-1519.
27. Jay T.M. Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 2003, 69:375-390.
28. Kalivas P.W. Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Brain Res Rev 1993, 18:75-113.
29. Kalivas P.W., Duffy P. D1 receptors modulate glutamate transmission in the ventral tegmental area. J Neurosci 1995, 15:5379-5388.
30. Kim J.J., Baxter M.G. Multiple brain-memory systems: the whole does not equal the sum of its parts. Trends Neurosci 2001, 24:324-330.
31. Kim Y.B., Matthews M., Moghaddam B. Putative γ-aminobutyric acid neurons in the ventral tegmental area have a similar pattern of plasticity as dopamine neurons during appetitive and aversive learning. Eur J Neurosci 2010, 32:1564-1572.
32. Kotecha S.A., Oak J.N., Jackson M.F., Perez Y., Orser B.A., Van Tol H.H., MacDonald J.F. A D2 class dopamine receptor transactivates a receptor tyrosine kinase to inhibit NMDA receptor transmission. Neuron 2002, 35:1111-1122.
33. Kretschmer B.D. Modulation of the mesolimbic dopamine system by glutamate: role of NMDA receptors. J Neurochem 1999, 73:839-848.
34. Lisman J.E., Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 2005, 46:703-713.
35. Lu X.Y., Churchill L., Kalivas P.W. Expression of D1 receptor mRNA in projections from the forebrain to the ventral tegmental area. Synapse 1997, 25:205-214.
36. Mahmoodi M., Shahidi S., Hasanein P. Involvement of the ventral tegmental area in the inhibitory avoidance memory in rats. Physiol Behav 2011, 28:542-547.
37. Managò F., Castellano C., Oliverio A., Mele A., De Leonibus E. Role of dopamine receptors subtypes, D1-like and D2-like, within the nucleus accumbens subregions, core and shell, on memory consolidation in the one-trial inhibitory avoidance task. Learn Mem 2009, 16:46-52.
38. Mao J.B., Robinson J.K. Microinjection of GABA-A agonist muscimol into the dorsal but not the ventral hippocampus impairs non-mnemonic measures of delayed non-matching-to-position performance in rats. Brain Res 1998, 784:139-147.
39. Martig A.K., Jones G.L., Smith K.E., Mizumori S.J. Context dependent effects of ventral tegmental area inactivation on spatial working memory. Behav Brain Res 2009, 203:316-320.
40. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: from structure to function. Physiol Rev 1998, 78:189-225.
41. Moser M.B., Moser E.I. Distributed encoding and retrieval of spatial memory in the hippocampus. J Neurosci 1998, 18:7535-7542.
42. Myhrer T. Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brain Res Brain Res Rev 2003, 41:268-287.
43. Nadel L., Samsonovich A., Ryan L., Moscovitch M. Multiple trace theory of human memory: computational, neuroimaging, and neuropsychological results. Hippocampus 2000, 10:352-368.
44. Nguyen P.V., Abel T., Kandel E.R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science 1994, 265:1104-1107.
45. O'Carroll C.M., Martin S.J., Sandin J., Frenguelli B., Morris R.G. Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learn Mem 2006, 13:760-769.
46. O'Donnell P. Dopamine gating of forebrain neural ensembles. Eur J Neurosci 2003, 17:429-435.
47. Paulsen O., Moser E.I. A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci 1998, 21:273-278.
48. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press, San Diego, CA.
49. Pettit D.L., Augustine G.J. Distribution of functional glutamate and GABA receptors on hippocampal pyramidal cells and interneurons. J Neurophysiol 2000, 84:28-38.
50. Phelps E.A. Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 2004, 14:198-202.
51. Rezayof A., Habibi P., Zarrindast M.R. Involvement of dopaminergic and glutamatergic systems of the basolateral amygdale in amnesia induced by the stimulation of dorsal hippocampal cannabinoid receptors. Neurosience 2011, 175:118-126.
52. Rezayof A., Motevasseli T., Rassouli Y., Zarrindast M.R. Dorsal hippocampal dopamine receptors are involved in mediating ethanol state-dependent memory. Life Sci 2007, 80:285-292.
53. Richter-Levin G. The amygdala, the hippocampus and emotional modulation of memory. Neuroscientist 2004, 10:131-139.
54. Saito S., Okada A., Ouwa T., Kato A., Akagi M., Kamei C. Interaction between hippocampal gama-aminobutyric acid(A) and N-methyl-d-aspartate receptors in the retention of spatial working memory in rats. Biol Pharm Bull 2010, 33:439-443.
55. Seamans J.K., Floresco S.B., Phillips A.G. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. J Neurosci 1998, 18:1613-1621.
56. Sharf R., Lee D.Y., Ranaldi R. Microinjections of SCH 23390 in the ventral tegmental area reduce operant responding under a progressive ratio schedule of food reinforcement in rats. Brain Res 2005, 1033:179-185.
57. Shohamy D., Wagner A.D. Integrating memories in the human brain: hippocampal-midbrain encoding of overlapping events. Neuron 2008, 60:378-389.
58. Sieghart W., Fuchs K., Tretter V., Ebert V., Jechlinger M., Höger H., Adamiker D. Structure and subunit composition of GABA(A) receptors. Neurochem Int 1999, 34:379-385.
59. Stuchlik A., Vales K. Effect of dopamine D1 receptor antagonist SCH23390 and D1 agonist A77636 on active allothetic place avoidance, a spatial cognition task. Behav Brain Res 2006, 172:250-255.
60. Takahashi H., Kato M., Takano H., Arakawa R., Okumura M., Otsuka T., Kodaka F., Hayashi M., Okubo Y., Ito H., Suhara T. Differential contributions of prefrontal and hippocampal dopamine D(1) and D(2) receptors in human cognitive functions. J Neurosci 2008, 28:12032-12038.
61. Tran A.H., Uwano T., Kimura T., Hori E., Katsuki M., Nishijo H., Ono T. Dopamine D1 receptor modulates hippocampal representation plasticity to spatial novelty. J Neurosci 2008, 28:13390-13400.
62. Vallone D., Picetti R., Borrelli E. Structure and function of dopamine receptors. Neurosci Biobehav Rev 2000, 24:125-132.
63. Vianna M.R., Izquierdo L.A., Barros D.M., de Souza M.M., Rodrigues C., Sant'Anna M.K., Medina J.H., Izquierdo I. Pharmacological differences between memory consolidation of habituation to an open field and inhibitory avoidance learning. Braz J Med Biol Rres 2001, 34:233-240.
64. Voller J., Donek A., Cendelń J., Korelusová I., Vozeh F. The effect of D1-like receptor blockade on motor functions and spatial learning in B6CBA mice. Prague Med Rep 2008, 109:32-39.
65. Westerink B.H., Enrico P., Feimann J., De Vries J.B. The pharmacology of mesocortical dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and prefrontal cortex of the rat brain. J Pharmacol Exp Ther 1998, 285:143-154.
66. Westerink B.H., Kwint H.F., deVries J.B. The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci 1996, 76:2605-2611.
67. Yang S.N. Sustained enhancement of AMPA receptor- and NMDA receptor-mediated currents induced by dopamine D1/D5 receptor activation in the hippocampus: an essential role of postsynaptic Ca2+. Hippocampus 2000, 10:57-63.
68. Yoon T., Okada J., Jung M.W., Kim J.J. Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn Mem 2008, 15:97-105.
69. Young A.B., Chu D. Distribution of GABA-A and GABA-B receptors in mammalian brain: potential targets for drug development. Drug Dev Res 1990, 21:161-167.
70. Zarrindast M.R., Bakhsha A., Rostami P., Shafaghi B. Effects of intrahippocampal injection of GABAergic drugs on memory retention of passive avoidance learning in rats. J Psychopharmacol 2002, 16:313-319.
71. Zarrindast M.R., Noorbakhshnia M., Motamedi F., Haeri-Rohani A., Rezayof A. Effect of the GABAergic system on memory formation and state-dependent learning induced by morphine in rats. Pharmacology 2005, 76:93-100.
72. Zornoza T., Cano-Cebrián M.J., Martínez-García F., Polache A., Granero L. Hippocampal dopamine receptors modulate cFos expression in the rat nucleus accumbens evoked by chemical stimulation of the ventral hippocampus. Neuropharmacology 2005, 49:1067-1076.
73. Zornoza T., Cano-Cebrián M.J., Miquel M., Aragón C., Polache A., Granero L. Hippocampal dopamine receptors modulate the motor activation and the increase in dopamine levels in the rat nucleus accumbens evoked by chemical stimulation of the ventral hippocampus. Neuropsychopharmacology 2005, 30:843-852.