Acquisition and expression of conditioned taste aversion differentially affects extracellular signal regulated Kinase and glutamate receptor phosphorylation in rat prefrontal cortex and nucleus accumbens

Frontiers in Behavioral Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Marotta, Roberto ^a   Fenu, Sandro ^b   Scheggi, Simona ^b,c   Vinci, Stefania ^b   Rosas, Michela ^b,c   Falqui, Andrea ^a   Gambarana, Carla ^b,c   De Graziella, M Graziella ^b,c   Acquas, Elio ^b,c  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c UNIVERSITY OF SIENA   (Italy)

Author keywords

Conditioned taste aversion (CTA); Extracellular signal regulated kinase (ERK); Glutamate receptors; Immuno electron microscopy; Nucleus accumbens (Acb); Prefrontal cortex (PFCx)

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 1; LITHIUM CHLORIDE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PHOSPHOPROTEIN DARPP 32; SODIUM CHLORIDE; THREONINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONDITIONED TASTE AVERSION; CONTROLLED STUDY; ENZYME ACTIVATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; IMMUNOGOLD STAINING; MALE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RAT; STATE DEPENDENT LEARNING; SUGAR INTAKE; TASTE AVERSION;

EID: 84900441053     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00153     Document Type: Article

References (76)

1. Acquas, E., Carboni, E., Leone, P., and Di Chiara, G. (1989). SCH 23390 blocks drug-conditioned place-preference and place-aversion: anhedonia (lack of reward) or apathy (lack of motivation) after dopamine-receptor blockade? Psychopharmacology 99, 151-155. doi: 10.1007/BF00442800
2. Acquas, E., and Di Chiara, G. (1994). D1 receptor blockade stereospecifically impairs the acquisition of drug-conditioned place preference and place aversion. Behav. Pharmacol. 5, 555-569. doi: 10.1097/00008877-199410000-00001
3. Acquas, E., Pisanu, A., Spiga, S., Plumitallo, A., Zernig, G., and Di Chiara, G. (2007). Differential effects of intravenous R,S-(+/-)-3,4-methylenedioxymethamphetamine (MDMA, Ecstasy) and its S(+)- and R(-)-enantiomers on dopamine transmission and extracellular signal regulated kinase phosphorylation (pERK) in the rat nucleus accumbens shell and core. J. Neurochem. 102, 121-132. doi: 10.1111/j.1471-4159.2007.04451.x
4. Acquas, E., Vinci, S., Fenu, S., De Montis, M. G., Gambarana, C., Scheggi, S., et al. (2011). Conditioned taste aversion elicited ERK activation and changes of dendritic spines density: an immunohistochemical, Golgi-Cox and electron microscopy study. Behav. Pharmacol. 22(Suppl. S), E38-E38.
5. Akirav, I. (2007). NMDA Partial agonist reverses blocking of extinction of aversive memory by GABA(A) agonist in the amygdala. Neuropsychopharmacology 32, 542-550. doi: 10.1038/sj.npp.1301050
6. Barki-Harrington, L., Elkobi, A., Tzabary, T., and Rosenblum, K. (2009). Tyrosine phosphorylation of the 2B subunit of the NMDA receptor is necessary for taste memory formation. J. Neurosci. 29, 9219-9226. doi: 10.1523/JNEUROSCI.5667-08.2009
7. Bassareo, V., De Luca, M. A., and Di Chiara, G. (2002). Differential expression of motivational stimulus properties by dopamine in nucleus accumbens shell versus core and prefrontal cortex. J. Neurosci. 22, 4709-4719.
8. Berendse, H. W., and Groenewegen, H. J. (1990). Organization of the thalamos-triatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol. 299, 187-228. doi: 10.1002/cne.902990206
9. Berman, D. E., Hazvi, S., Rosenblum, K., Seger, R., and Dudai, Y. (1998). Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J. Neurosci. 18, 10037-10044.
10. Bernstein, I. L., and Koh, M. T. (2007). Molecular signaling during taste aversion learning. Chem. Senses 32, 99-103. doi: 10.1093/chemse/bjj032
11. Boggio, E. M., Putignano, E., Sassoè-Pognetto, M., Pizzorusso, T., and Giustetto, M. (2007). Visual stimulation activates ERK in synaptic and somatic compartments of rat cortical neurons with parallel kinetics. PLoS ONE 2:e604. doi: 10.1371/journal.pone.0000604
12. Brog, J. S., Salyapongse, A., Deutch, A. Y., and Zahm, D. S. (1993). The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluorogold. J. Comp. Neurol. 338, 255-278. doi: 10.1002/cne.903380209
13. Cannon, C. M., Scannell, C. A., and Palmiter, R. D. (2005). Mice lacking dopamine D1 receptors express normal lithium chloride-induced conditioned taste aversion for salt but not sucrose. Eur. J. Neurosci. 21, 2600-2604. doi: 10.1111/j.1460-9568.2005.04077.x
14. Cardinal, R. N., Parkinson, J. A., Hall, J., and Everitt, B. J. (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321-352. doi: 10.1016/S0149-7634(02) 00007-6
15. Cui, Z., Lindl, K. A., Mei, B., Zhang, S., and Tsien, J. Z. (2005). Requirement of NMDA receptor reactivation for consolidation and storage of nondeclara-tive taste memory revealed by inducible NR1 knockout. Eur. J. Neurosci. 22, 755-763. doi: 10.1111/j.1460-9568.2005.04257.x
16. Danielli, B., Scheggi, S., Grappi, S., Marchese, G., De Montis, M. G., Tagliamonte, A., et al. (2010). Modifications in DARPP-32 phosphorylation pattern after repeated palatable food consumption undergo rapid habituation in the nucleus accumbens shell of non-food-deprived rats. J. Neurochem. 112, 531-541. doi: 10.1111/j.1471-4159.2009.06483.x
17. Di Chiara, G. (2002). Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res. 137, 75-114. doi: 10.1016/S0166-4328(02)00286-3
18. Dunn, L. T., and Everitt, B. J. (1988). Double dissociations of the effects of amygdala and insular cortex lesions on conditioned taste aversion, passive avoidance, and neophobia in the rat using the excitotoxin ibotenic acid. Behav. Neurosci. 102, 3-23. doi: 10.1037/0735-7044.102.1.3
19. Elkobi, A., Ehrlich, I., Belelovsky, K., Barki-Harrington, L., and Rosenblum, K. (2008). ERK-dependent PSD-95 induction in the gustatory cortex is necessary for taste learning, but not retrieval. Nat. Neurosci. 11, 1149-1151. doi: 10.1038/nn.2190
20. Fasano, S., and Brambilla, R. (2011). Ras-ERK signaling in behavior: old questions and new perspectives. Front. Behav. Neurosci. 5:79. doi: 10.3389/fnbeh.2011.00079
21. Fenu, S., Bassareo, V., and Di Chiara, G. (2001). A role for dopamine D1 receptors of the nucleus accumbens shell in conditioned taste aversion learning. J. Neurosci. 21, 6897-6904.
22. Fenu, S., Cadoni, C., and Di Chiara, G. (2010). Conditioned saccharin avoidance and sensitization to drugs of abuse. Behav. Brain Res. 214, 248-253. doi: 10.1016/j.bbr.2010.05.044
23. Fenu, S., and Di Chiara, G. (2003). Facilitation of conditioned taste aversion learning by systemic amphetamine: role of nucleus accumbens shell dopamine D1 receptors. Eur. J. Neurosci. 18, 2025-2030. doi: 10.1046/j.1460-9568.2003.02899.x
24. Fenu, S., Rivas, E., and Di Chiara, G. (2005). Differential role of dopamine in drug-and lithium conditioned saccharin avoidance. Physiol. Behav. 85, 37-43. doi: 10.1016/j.physbeh.2005.04.002
25. Fenu, S., Rivas, E., and Di Chiara, G. (2009). Differential involvement of dopamine D1 receptors in morphine- and lithium-conditioned saccharin avoidance. Physiol. Behav. 96, 73-77. doi: 10.1016/j.physbeh.2008.08.017
26. Ferreira, G., Ferry, B., Meurisse, M., and Lévy, F. (2006). Forebrain structures specifically activated by conditioned taste aversion. Behav. Neurosci. 120, 952-962. doi: 10.1037/0735-7044.120.4.952
27. Garcia, J., Kimeldorf, D. J., and Koelling, R. A. (1955). Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122, 157-158.
28. Gilmartin, M. R., and Helmstetter, F. J. (2010). Trace and contextual fear conditioning require neural activity and NMDA receptor-dependent transmission in the medial prefrontal cortex. Learn. Mem. 17, 289-296. doi: 10.1101/lm.15 97410
29. Girault, J. A., Valjent, E., Caboche, J., and Hervé, D. (2007). ERK2: a logical AND gate critical for drug-induced plasticity? Curr. Opin. Pharmacol. 7, 77-85. doi: 10.1016/j.coph.2006.08.012
30. Greenshaw, A. J., and Buresová, O. (1982). Learned taste aversion to saccharin following intraventricular or intraperitoneal administration of d,l-amphetamine. Pharmacol. Biochem. Behav. 17, 1129-1133. doi: 10.1016/0091-3057(82) 90107-1
31. Groenewegen, H. J., Berendse, H. W., Wolters, J. G., and Lohman, A. H. M. (1990). "The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization," in Progress in Brain Research, Vol. 85, eds H. B. M. Uylings, C. G. VanEden, J. P. C. DeBruin, M. A. Corner, and M. G. P. Feenstra (Amsterdam: Elsevier Science Publishers), 95-118.
32. Guzmán-Ramos, K., Osorio-Gómez, D., Moreno-Castilla, P., and Bermúdez-Rattoni, F. (2010). Off-line concomitant release of dopamine and glu-tamate involvement in taste memory consolidation. J. Neurochem. 114, 226-236. doi: 10.1111/j.1471-4159.2010.06758.x
33. Hardingham, G. E., Arnold, F. J., and Bading, H. (2001). A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat. Neurosci. 4, 565-566. doi: 10.1038/88380
34. Heidbreder, C. A., and Groenewegen, H. J. (2003). The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27, 555-579. doi: 10.1016/j.neubiorev.2003.09.003
35. Hoffman, D. C., and Beninger, R. J. (1988). Selective D1 and D2 dopamine agonists produce opposing effects in place conditioning but not in conditioned taste aversion learning. Pharmacol. Biochem. Behav. 31, 1-8. doi: 10.1016/0091-3057(88)90302-4
36. Humbel, B. M., and Schwartz, H. (1989). "Freeze-substitution for immunochem-istry," in Immunogold Labelling in Cell Biology, eds A. J.Verkleij and J. L. M. Leunissen (Boca Raton, FL: CRC Press), 115-134.
37. Ibba, F., Vinci, S., Spiga, S., Peana, A. T., Assaretti, A. R., Spina, L., et al. (2009). Ethanol-induced extracellular signal regulated kinase: role of dopamine D1 receptors. Alcohol Clin. Exp. Res. 33, 858-867. doi: 10.1111/j.1530-0277.2009.00907.x
38. Inui, T., Inui-Yamamoto, C., Yoshioka, Y., Ohzawa, I., and Shimura, T. (2013). Activation of efferents from the basolateral amygdala during the retrieval of conditioned taste aversion. Neurobiol. Learn. Mem. 106, 210-220. doi: 10.1016/j.nlm.2013.09.003
39. Inui-Yamamoto, C., Yoshioka, Y., Inui, T., Sasaki, K. S., Ooi, Y., Ueda, K., et al. (2010). The brain mapping of the retrieval of conditioned taste aversion memory using manganese-enhanced magnetic resonance imaging in rats. Neuroscience 167, 199-204. doi: 10.1016/j.neuroscience.2010.02.027
40. Kapur, J. N., Sahoo, P. K., and Wong, K. C. (1985). A new method for gray-level picture thresholding using the entropy of the histogram. Comput. Vis. Graph. Image Process. 29, 273-285. doi: 10.1016/0734-189X(85)90125-2
41. Kwon, B., and Houpt, T. A. (2012). Mitogen-activated protein kinase in the amygdala plays a critical role in lithium chloride-induced taste aversion learning. Neurobiol. Learn. Mem. 97, 132-139. doi: 10.1016/j.nlm.2011. 10.005
42. Languille, S., Davis, S., Richer, P., Alcacer, C., Laroche, S., and Hars, B. (2009). Extracellular signal-regulated kinase activation is required for consolidation and reconsolidation of memory at an early stage of ontogenesis. Eur. J. Neurosci. 30, 1923-1930. doi: 10.1111/j.1460-9568.2009.06971.x
43. Lin, P. Y., Wang, S. P., Tai, M. Y., and Tsai, Y. F. (2010). Differential involvement of medial prefrontal cortex and basolateral amygdala extracellular signal-regulated kinase in extinction of conditioned taste aversion is dependent on different intervals of extinction following conditioning. Neuroscience 171, 125-133. doi: 10.1016/j.neuroscience.2010.08.066
44. Liu, J. P., Liu, Y. Y., Wong-Riley, M. T. T., Liu, H. J., and Ju, G. (2005). A group of neurokinin-1 receptor-immunoreactive neurons expressing phospho-extracellular signal-regulated protein kinases in the pre-Bötzinger complex of rats. J. Neurosci. Res. 80, 260-267. doi: 10.1002/jnr.20445
45. Longoni, R., Spina, L., Vinci, S., and Acquas, E. (2011). The MEK inhibitor SL327 blocks acquisition but not expression of lithium-induced conditioned place aversion: a behavioral and immunohistochemical study. Psychopharmacology 216, 63-73. doi: 10.1007/s00213-011-2192-9
46. Mark, G. P., Blander, D. S., and Hoebel, B. G. (1991). A conditioned stimulus decreases Extracellular dopamine in the nucleus accumbens after the development of a learned taste aversion. Brain Res. 551, 308-310. doi: 10.1016/0006-8993(91)90946-S
47. Mathiisen, T. M., Nagelhus, E. A., Jouleh, B., Torp, R., Frydenlund, D. S., Mylonakou, M. N., et al. (2006). "Postembedding immunogold cytochemistry of membrane molecules and amino acid transmitters in the central nervous system," in Neuroanatomical Tract-Tracing 3: Molecules, Neurons, and Systems, eds L. Zaborszky, F. G. Wouterlood, and J. L. Lanciego (New York, NY: Springer), 72-108. doi: 10.1007/0-387-28942-9_3
48. McGaugh, J. L. (2000). Memory-a century of consolidation. Science 287, 248-251. doi: 10.1126/science.287.5451.248
49. Mickley, G. A., Kenmuir, C. L., Yocom, A. M., Wellman, J. A., and Biada, J. M. (2005). A role for prefrontal cortex in the extinction of a conditioned taste aversion. Brain Res. 1051, 176-182. doi: 10.1016/j.brainres.2005. 05.033
50. Nagai, T., Takuma, K., Kamei, H., Ito, Y., Nakamichi, N., Ibi, D., et al. (2007). Dopamine D1 receptors regulate protein synthesis-dependent long-term recognition memory via extracellular signal-regulated kinase 1/2 in the prefrontal cortex. Learn Mem. 14, 117-125. doi: 10.1101/lm.461407
51. Núñez-Jaramillo, L., Rangel-Hernández, J. A., Burgueño-Zúñiga, B., and Miranda, M. I. (2012). Activation of nucleus accumbens NMDA receptors differentially affects appetitive or aversive taste learning and memory. Front. Behav. Neurosci. 6:13. doi: 10.3389/fnbeh.2012.00013
52. Oprins, A., Geuze, H. J., and Slot, J. W. (1994). Cryosubstitution dehydration of aldehyde-fixed tissue: a favorable approach to quantitative immunocytochem-istry. J. Histochem. Cytochem. 42, 497-503. doi: 10.1177/42.4.8126376
53. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates, 4th Edn. San Diego, CA: Academic Press.
54. Rácz, B., Blanpied, T. A., Ehlers, D. E., and Weinberg, R. J. (2004). Lateral organization of endocytic machinery in dendritic spines. Nat. Neurosci. 7, 917-918. doi: 10.1038/nn1303
55. Ramírez-Lugo, L., Núñez-Jaramillo, L., and Bermúdez-Rattoni, F. (2007). Taste memory formation: role of nucleus accumbens. Chem. Senses 32, 93-97. doi: 10.1093/chemse/bjl023
56. Rauggi, R., Scheggi, S., Cassanelli, A., De Montis, M. G., Tagliamonte, A., and Gambarana, C. (2005). The mesolimbic dopaminergic response to novel palatable food consumption increases dopamine-D1 receptor-mediated signalling with complex modifications of the DARPP-32 phosphoryla-tion pattern. J. Neurochem. 92, 867-877. doi: 10.1111/j.1471-4159.2004. 02920.x
57. Rosenblum, K., Berman, D. E., Hazvi, S., Lamprecht, R., and Dudai, Y. (1997). NMDA receptor and the tyrosine phosphorylation of its 2B subunit in taste learning in the rat insular cortex. J. Neurosci. 17, 5129-5135.
58. Runyan, J. D., and Dash, P. K. (2004). Intra-medial prefrontal administration of SCH-23390 attenuates ERK phosphorylation and long-term memory for trace fear conditioning in rats. Neurobiol. Learn. Mem. 82, 65-70. doi: 10.1016/j.nlm.2004.04.006
59. Scheggi, S., Raone, A., De Montis, M. G., Tagliamonte, A., and Gambarana, C. (2007). Behavioral expression of cocaine sensitization in rats is accompanied by a distinct pattern of modifications in the PKA/DARPP-32 signaling pathway. J. Neurochem. 103, 1168-1183. doi: 10.1111/j.1471-4159.2007. 04818.x
60. Scott, T. R. (2011). Learning through the taste system. Front. Syst. Neurosci. 5:87. doi: 10.3389/fnsys.2011.00087
61. Sétáló, G., Singh, M., Guan, X., and Toran-Allerand, C. D. (2001). Cellular localization of estradiol-induced phospho-ERK1/2 in mouse cerebral cortical explants: the roles of heat shock protein 90 and MEK2. J. Neurobiol. 50, 1-12. doi: 10.1002/neu.10000
62. Shiflett, M. W., and Balleine, B. W. (2011). Molecular substrates of action control in cortico-striatal circuits. Prog. Neurobiol. 95, 1-13. doi: 10.1016/j.pneurobio.2011.05.007
63. Simonyi, A., Serfozo, P., Parker, K. E., Ramsey, A. K., and Schachtman, T. R. (2009). Metabotropic glutamate receptor 5 in conditioned taste aversion learning. Neurobiol. Learn. Mem. 92, 460-463. doi: 10.1016/j.nlm.2009.05.002
64. Sindreu, C. B., Scheiner, Z. S., and Storm, D. R. (2007). Ca(2+)-Stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 53, 79-89. doi: 10.1016/j.neuron.2006.11.024
65. Sosinsky, G. E., Crum, J., Ying, Z. J., Lanman, J., Smarr, B., Terada, M., et al. (2008). The combination of chemical fixation with high pressure freezing and freeze substitution preserves highly labile tissue ultrastructure for electron tomography applications. J. Struct. Biol. 161, 359-371. doi: 10.1016/j.jsb.2007. 09.002
66. Suzuki, T., Mitake, S., and Murata, S. (1999). Presence of up-stream and downstream -Brain Res. 840, 36-44. doi: 10.1016/S0006-8993(99)01762-X
67. Suzuki, T., Okumura-Noji, K., and Nishida, E. (1995). ERK2-type mitogen activated protein kinase (MAPK) and its substrates in postsynaptic density fractions from the rat brain. Neurosci. Res. 22, 277-285. doi: 10.1016/0168-0102(95)00902-6
68. Valjent, E., Pascoli, V., Svenningsson, P., Paul, S., Enslen, H., Corvol, J. C., et al. (2005). Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc. Natl. Acad. Sci. U.S.A. 102, 491-496. doi: 10.1073/pnas.0408305102
69. van Genderen, I. L., van Meer, G., Slot, J. W., Geuze, H. J., and Voorhout, W. F. (1991). Subcellular localization of Forssman glycolipid in epithelial MDCK cells by immuno-electronmicroscopy after freeze-substitution. J. Cell Biol. 115, 1009-1019. doi: 10.1083/jcb.115.4.1009
70. van Lookeren Campagne, M., Oestreicher, A. B., van der Krift, T. P., Gispen, W. H., and Verkleij, A. J. (1991). Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens. J. Histochem. Cytochem. 39, 1267-1279. doi: 10.1177/39.9.18 33448
71. Xia, Z., Dudek, H., Miranti, C. K., and Greenberg, M. E. (1996). Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16, 5425-5436.
72. Xiao, B., Han, F., Wang, H. T., and Shi, Y. X. (2011). Single-prolonged stress induces increased phosphorylation of extracellular signal-regulated kinase in a rat model of post-traumatic stress disorder. Mol. Med. Rep. 4, 445-449. doi: 10.3892/mmr.2011.459
73. Yamamoto, T., Fujimoto, Y., Shimura, T., and Sakai, N. (1995). Conditioned taste aversion in rats with excitotoxic brain lesions. Neurosci. Res. 22, 31-49. doi: 10.1016/0168-0102(95)00875-T
74. Yasoshima, Y., Morimoto, T., and Yamamoto, T. (2000). Different disruptive effects on the acquisition and expression of conditioned taste aversion by blockades of amygdalar ionotropic and metabotropic glutamatergic receptor subtypes in rats. Brain Res. 869, 15-24. doi: 10.1016/S0006-8993(00) 02397-0
75. Yasoshima, Y., Scott, T. R., and Yamamoto, T. (2006). Memory-dependent c-Fos expression in the nucleus accumbens and extended amygdala following the expression of a conditioned taste aversive in the rat. Neuroscience 141, 35-45. doi: 10.1016/j.neuroscience.2006.03.019
76. Zhu, J. H., Fengli, G., Shelburne, J., Watkins, S., and Chu, C. T. (2006). Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in lewy body diseases. Brain Pathol. 13, 473-481. doi: 10.1111/j.1750-3639.2003.tb00478.x