Differential effects of neurotoxin-induced lesions of the basolateral amygdala and central nucleus of the amygdala on lithium-induced conditioned disgust reactions and conditioned taste avoidance

Behavioural Brain Research

Volumn 189, Issue 2, 2008, Pages 284-297

  Rana, Shadna A ^a   Parker, Linda A ^b  

^a WILFRID LAURIER UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Amygdala; Conditioned disgust; Fear; Illness; Lesion; Lithium; Nausea; Neurotoxin; Taste avoidance; Taste reactivity

Indexed keywords

LITHIUM; NEUROTOXIN; SACCHARIN;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BASOLATERAL AMYGDALA; BASOLATERAL MEMBRANE; BRAIN REGION; CENTRAL NUCLEUS AMYGDALA; CONDITIONING; CONTROLLED STUDY; IMAGE DISPLAY; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TASTE AVERSION;

AMYGDALA; ANIMALS; ASSOCIATION LEARNING; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; EXCITATORY AMINO ACID AGONISTS; FLAVORING AGENTS; LITHIUM CHLORIDE; MALE; NAUSEA; RATS; RATS, SPRAGUE-DAWLEY; TASTE;

EID: 41149147461     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.01.005     Document Type: Article

References (73)

1. Bahar A., Samuel A., Hazvi S., and Dudai Y. The amygdalar circuit that acquires taste aversion memory differs from the circuit that extinguishes it. Eur J Neurosci 17 (2003) 1527-1530
2. Batsell Jr. W.R., and Best M.R. One bottle too many? Method of testing determines the detection of overshadowing and retention of taste aversions. Anim Learn Behav 2 (1993) 154-158
3. Berger B.D. Conditioning of food aversions by injections of psychoactive drugs. J Comp Physiol Psychol 8 (1972) 21-26
4. Bermudez-Rattoni F., and McGaugh J.L. Insular cortex and amygdala lesions. Differentially affect acquisition on inhibitory avoidance and conditioned taste aversion. Brain Res 549 (1991) 165-170
5. Bernstein I.L., and Koh M.T. Molecular signaling during taste aversion learning. Chem Senses 32 (2007) 99-103
6. Berridge K., Grill H.J., and Norgren R. Relation of consummatory responses and preabsorptive insulin release to palatability and learned taste aversions. J Comp Physiol Psychol 95 (1981) 363-382
7. Campeau S., and Davis M. Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 15 (1995) 2301-2311
8. Darmani N.A. Delta-9-tetrahydrocannabinol and synthetic cannabinoids prevent emesis produced by the cannabinoid CB1 receptor antagonist/inverse agonist SR-41716A. Neuropsychopharmacology 24 (2001) 198-203
9. Darmani N.A. Delta-9-tetrahydrocannabinoid differentially suppresses cisplatin-induced emesis and indices of motor function via cannabinoid CB1 receptors in the least shrew. Pharmacol Biochem Behav 69 (2001) 239-249
10. Darmani N.A. The cannabinoid CB1 receptor antagonist SR 131716A reverses the antiemetic and motor depressant actions of WIN 55, 212-2. Eur J Pharmacol 430 (2001) 49-58
11. Darmani N.A. The potent emetogenic effects of the endocannabinoid, 2-AG (2- arachidonoylglycerol) are blocked by delta(9)-tetrahydrocannabinol and other annabinoids. J Pharmacol Exp Ther 300 (2002) 34-42
12. Davis C.J., Harding R.K., Leslie R.A., and Andrews P.L.R. The organization of vomiting as a protective reflex. In: Davis C.J., Lake-Bakaar G.V., and Grahame-Smith D.G. (Eds). Nausea and vomiting: mechanisms and treatment (1986), Springer-Verlag, Berlin 65-75
13. Dunn L.T., and Everitt B.J. Double dissociation 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. Beh Neurosci 102 (1988) 3-23
14. Everitt B.J., Cardinal R.N., Parkinson J.A., and Robbins T.W. Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning. Ann N Y Acad Sci 985 (2003) 233-250
15. Fanselow M.S., and Gale G.D. The amygdala, fear, and memory. Ann N Y Acad Sci 985 (2003) 125-134
16. Ferreira G., Ferry B., Meurisse M., and Levy F. Forebrain structures specifically activated by conditioned taste aversion. Behav Neurosci 120 (2006) 952-962
17. Galaverna O.G., Seeley R.J., Berridge K.C., Grill H.J., Epstein A.N., and Schulkin J. Lesions of the central nucleus of the amygdala. I. Effects on taste reactivity, taste aversion learning and sodium appetite. Behav Brain Res 59 (1993) 11-17
18. Gamzu E. The multifaceted nature of taste aversion inducing agents: is there a single common factor?. In: Baker L.M., Domjan M., and Best M.R. (Eds). Learning mechanisms of food selection (1977), Baylor University Press, Waco 447-511
19. Garcia J., Hankins W.G., and Rusiniak K.W. Behavioral regulation of the milieu interne in man and rat. Science 185 (1974) 824-831
20. Goosens K.A., and Maren S. Contextual and auditory fear conditioning are mediated by the lateral, basal, and central amygdaloid nuclei in rats. Learn Mem 8 (2001) 148-155
21. Grigson P.S. Conditioned taste aversions and drugs of abuse: a reinterpretation. Behav Neurosci 111 (1997) 129-136
22. Grill H.C., and Norgren R. The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143 (1978) 263-279
23. Honore T., Krogsgaard-Larsen P., Hansen J.J., and Lauridsen J. Glutamate and aspartate agonists structurally related to ibotenic acid. Mol Cell Biochem 38 (1981) 123-128
24. Hunt T., and Amit Z. Conditioned taste aversion by self-administered drugs: paradox revisited. Neurosci Biobehav Rev 11 (1987) 107-130
25. Kemble E.D., Studelska D.R., and Schmidt M.K. Effects of central amygdaloid nucleus lesions on ingestion, taste reactivity, exploration and taste aversion. Physiol Behav 22 (1979) 789-793
26. Kiefer S.W., and Orr M.R. Taste avoidance, but not aversion, learning in rats lacking gustatory cortex. Behav Neurosci 106 (1992) 140-146
27. Killcross S., Robbins T.W., and Everitt B.J. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature 388 (1997) 377-380
28. Koh M.T., Wilkins E.E., and Bernstein I.L. Novel tastes elevate c-fos expression in the central amygdala and insular cortex: implication for taste aversion learning. Behav Neurosci 117 (2003) 1416-1422
29. Koo J.W., Han J.S., and Kim J.J. Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. J Neurosci 24 (2004) 7654-7662
30. Kwiatkowska M., and Parker L.A. Ondansetron and Delta-9-tetrahydrocannabinol interfere with the establishment of lithium-induced conditioned taste avoidance in the house musk shrew (Suncus murinus). Behav Neurosc 119 (2005) 974-982
31. Lamprecht R., and Dudai Y. Differential modulation of brain immediate early genes by intraperitoneal LiCl. Neuroreport 7 (1995) 289-293
32. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 23 (2000) 155-184
33. Lee Y., Walker D., and Davis M. Lack of a temporal gradient of retrograde amnesia following NMDA-induced lesions of the basolateral amygdala assessed with the fear-potentiated startle paradigm. Behav Neurosci 110 (1996) 836-839
34. Limebeer C.L., and Parker L.A. The antiemetic drug Ondansetron interferes with lithium-induced conditioned rejection reactions, but not lithium-induced taste avoidance in rats. J Exp Psychol Anim Behav Process 26 (2000) 371-384
35. Limebeer C.L., Parker L.A., and Fletcher P.J. 5,7-Dihydroxytryptamine lesions of the dorsal and median raphe nuclei interfere with lithium-induced conditioned gaping, but not conditioned taste avoidance, in rats. Behav Neurosci 118 (2004) 1391-1399
36. Lopez-Velazquez L., Aguirre E., and Paredes R.G. Kindling increases aversion to saccharin in taste aversion learning. Neuroscience 144 (2007) 808-814
37. McGowan B.K., Hankins W.G., and Garcia J. Limbic lesions and control of the internal and external environment. Behav Biol 7 (1972) 841-852
38. Melia K.R., Falls W.A., and Davis M. Involvement of pertussis toxin sensitive G-proteins in conditioned fear-potentiated startle: possible involvement of the amygdala. Brain Res 584 (1992) 141-148
39. Miranda M.I., Ferreira G., Ramirez-Lugo L., and Bermudez-Rattoni F. Glutamatergic activity in the amygdala signals visceral input during taste memory formation. Proc Natl Acad Sci USA 99 (2002) 11417-11422
40. Miranda M.I., LaLumiere R.T., Buen T.V., Bermudez-Rattoni F., and McGaugh J.L. Blockade of noradrenergic receptors in the basolateral amygdala impairs taste memory. Eur J Neurosci 18 (2003) 2010-2605
41. Monaghan D.T., and Cotman C.W. Distribution of N-methyl-d-aspartate-sensitive l-[3H]glutamate-binding sites in rat brain. J Neurosci 5 (1985) 2909-2919
42. Morris R., Frey S., Kasambira T., and Petrides M. Ibotenic acid lesions of the basolateral, but not the central, amygdala interfere with conditioned taste aversion: evidence from a combined behavioral and anatomical tract-tracing investigation. Behav Neurosci 113 (1999) 291-302
43. Nachman M., and Ashe J.H. Effects of basolateral amygdala lesions on neophobia, learned taste aversions, and sodium appetite in rats. J Comp Physiol Psychol 87 (1974) 622-643
44. Parker L.A. Nonconsummatory and consummatory behavioral CRs elicited by lithium- and amphetamine-paired flavors. Learn Motiv 13 (1982) 281-303
45. Parker L.A. Rewarding drugs produce taste avoidance, but not taste aversion. Neurosci Biobehav Rev 19 (1995) 143-151
46. Parker L.A. Taste avoidance and taste aversion: evidence for two different processes. Learn Behav 31 (2003) 165-172
47. Parker L.A., Corrick M.L., Limebeer C.L., and Kwiatkowska M. Amphetamine and morphine produce a conditioned taste and place preference in the house musk shrew (Suncus murinus). J Exp Psychol: Anim Behav Process 28 (2002) 75-82
48. Parker L.A., Kwiatkowska M., Burton P., and Mechoulam R. Effect of cannabinoids on lithium-induced vomiting in the Suncus murinus (house musk shrew). Psychopharmacology 171 (2004) 156-161
49. Parker L.A., Mechoulam R., Schlievert C., Abbott L.A., Fudge M.L., and Burton P. Cannabinoid agonists attenuate and a cannabinoid antagonist potentiates lithium-induced conditioned rejection reactions in a rat model of nausea. Psychopharmacology 166 (2003) 156-162
50. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. 4th ed. (1998), Academic Press, San Diego
51. Pelchat M.L., Grill H.J., Rozin P., and Jacobs J. Quality of acquired responses to tastes by Rattus norvegicus depends on type of associated discomfort. J Comp Psychol 97 (1983) 140-153
52. Reilly S., and Bornovalova M.A. Conditioned taste aversion and amygdala lesions in the rat: a critical review. Neurosci Biobehav Rev 29 (2005) 1067-1088
53. Revusky S.H., and Bedarf E.W. Association of illness with prior ingestion of novel foods. Science 155 (1967) 219-220
54. Rodriques G., and Alonso G. Latent inhibition as a function of CS intensity in taste aversion learning. Behav Processes 60 (2002) 61-67
55. Schafe G.E., Thiele T.E., and Bernstein I.L. Conditioning method dramatically alters the role of amygdala in taste aversion learning. Learn Mem 5 (1998) 481-492
56. Schoenfeld T.A., and Hamilton L.W. Disruption of appetite but not hunger or satiety following small lesions in the amygdala of rats. J Comp Physiol Psychol 95 (1981) 565-587
57. Selden N.R., Everitt B.J., Jarrard L.E., and Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 42 (1991) 335-350
58. Simoneau I.I., Hamza M.S., Mata H.P., Siegel E.M., Vanderah T.W., Porreca F., et al. The cannabinoid agonist WIN 55, 212-2 suppresses opioid-induced emesis in ferrets. Anesthesiology 94 (2001) 882-887
59. Smith J.E., Friedman M.I., and Andrews P.L.R. Conditioned food aversion in Suncus murinus (house musk shrew) a new model for the study of nausea in a species with an emetic reflex. Physiol Behav 73 (2001) 593-598
60. Spencer C.M., and Houpt T.A. Dynamics of c-fos and ICER mRNA expression in rat forebrain following lithium chloride injection. Brain Res Mol Brain Res 93 (2001) 113-126
61. St Andre J., and Reilly S. Effects of central and basolateral amygdala lesions on conditioned taste aversion and latent inhibition. Behav Neurosci 121 (2007) 90-99
62. St Andre J., Albanos K., and Reilly S. C-fos expression in the rat brain following lithium chloride-induced illness. Brain Res 1135 (2007) 122-128
63. Stone M.E., Grimes B.S., and Katz D.B. Hippocampal inactivation enhances taste learning. Learn Mem 12 (2005) 579-586
64. Touzani K., Taghzouti K., and Velley L. Increase of the aversive value of taste stimuli following ibotenic acid lesion of the central amygdaloid nucleus in the rat. Behav Brain Res 88 (1997) 133-142
65. Van Sickle M.D., Oland L.D., Ho W., Hillard C.J., Mackie K., Davison J.J., et al. Cannabinoids inhibit emesis through CB1 receptors in the brainsten of the ferret. Gastroenterology 121 (2001) 767-777
66. Watkins J.C., and Jane D.E. The glutamate story. Br J Pharmacol 147 suppl. 1 (2006) S100-S108
67. White N.M., and McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77 (2002) 125-184
68. Wilkins E.E., and Bernstein I.L. Conditioning method determines patterns of c-fos expression following novel taste-illness pairing. Behav. Brain Res 169 (2006) 93-97
69. Yamamoto T. Brain regions responsible for the expression of conditioned taste aversion in rats. Chem Senses 32 (2007) 105-109
70. Yamamoto T., Fujimoto Y., Shimura T., and Sakai N. Conditioned taste aversion in rats with excitotoxic brain lesions. Neurosci Res 22 (1995) 31-49
71. Yamamoto T., Sako N., Sakai N., and Iwafune A. Gustatory and visceral inputs to the amygdala of the rat: conditioned taste aversion and induction of c-fos-like immunoreactivity. Neurosci Lett 226 (1997) 127-130
72. Yamamoto T., Shimura T., Sako N., Yasoshima Y., and Sakai N. Neural substrates for conditioned taste aversion in the rat. Behav Brain Res 65 (1994) 123-137
73. Yamamoto T., Shimura T., Sako N., Azuma S., Bai W.Z., and Wakisaka S. C-fos expression in the rat brain after intraperitoneal injection of lithium chloride. Neuroreport 3 (1992) 1049-1052