Lipopolysaccharide dose dependently impairs rapid toxin (LiCl)-induced gustatory conditioning: A taste reactivity examination of the conditioned taste aversion

Brain, Behavior, and Immunity

Volumn 23, Issue 2, 2009, Pages 204-216

  Cross Mellor, Shelley K ^a   Foley, Kelly A ^a   Parker, Linda A ^b   Ossenkopp, Klaus Peter ^a  

^a Social Science Centre   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Cognitive abilities; Feeding; Immune stimulation; Ingestion; Learning; Locomotor activity; Memory

Indexed keywords

LIPOPOLYSACCHARIDE; SODIUM CHLORIDE; SUCROSE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL RESEARCH; CANNULA; CONCENTRATION RESPONSE; CONDITIONING; CONTROLLED STUDY; FLAVOR; FOOT; HABITUATION; IMMUNE RESPONSE; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TASTE AVERSION; TASTE DISCRIMINATION;

ADMINISTRATION, ORAL; ANIMALS; ASSOCIATION LEARNING; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CONDITIONING, OPERANT; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTOXINS; HABITUATION, PSYCHOPHYSIOLOGIC; LIPOPOLYSACCHARIDES; LITHIUM CHLORIDE; MALE; RATS; RATS, LONG-EVANS; SODIUM CHLORIDE; SUCROSE; TASTE;

EID: 58549085952     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2008.09.006     Document Type: Article

References (65)

1. Aubert A., and Dantzer R. The taste of sickness: lipopolysaccharide-induced finickiness in rats. Physiol. Behav. 84 (2005) 437-444
2. Aubert A., Vega C., Dantzer R., and Goodall G. Pyrogens specifically disrupt the acquisition of a task involving cognitive processing in the rat. Brain Behav. Immun. 9 (1995) 129-148
3. Barrientos R.M., Higgins E.A., Biedenkapp J.C., Sprunger D.B., Wright-Hardesty K.J., Watkins L.R., Rudy J.W., and Maier S.F. Peripheral infection and aging interact to impair hippocampal memory consolidation. Neurobiol. Aging 27 (2006) 723-732
4. Barrientos R.M., Higgins E.A., Sprunger D.B., Watkins L.R., Rudy J.W., and Maier S.F. Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav. Brain Res. 134 (2002) 291-298
5. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
6. Brennan F.X., Beck K.D., and Servatius R.J. Low doses of interleukin-1beta improve the leverpress avoidance performance of Sprague-Dawley rats. Neurobiol. Learn. Mem. 80 (2003) 168-171
7. Bsibsi M., Ravid R., Gveric D., and van Noort J.M. Broad expression of Toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 61 (2002) 1013-1021
8. Bures, J., Bermudez-Rattoni, F., Yamamoto, T., 1998. Conditioned taste aversion: memory of a special kind.
9. Commins S., O'Neill L.A.J., and O'Mara S.M. The effects of the bacterial endotoxin lipopolysaccharide on synaptic transmission and plasticity in the CA1-subiculum pathway in vivo. Neuroscience 102 (2001) 273-280
10. Cottrell G.A., and Nakajima S. Effect of corticosteroids in the hippocampus on passive avoidance behavior in the rat. Pharmacol. Biochem. Behav. 7 (1977) 277-280
11. Cross-Mellor S., Clarke S.N., and Ossenkopp K.-P. Rapid toxin-induced gustatory conditioning in rats: separate and combined effects of systemic injection or intraoral infusion of lithium chloride. Behav. Brain Res. 154 (2004) 423-430
12. Cross-Mellor S.K., Kavaliers M., and Ossenkopp K.-P. Comparing immune activation (lipopolysaccharide) and toxin (lithium chloride)-induced gustatory conditioning: lipopolysaccharide produces conditioned taste avoidance but not aversion. Behav. Brain Res. 148 (2004) 11-19
13. Cross-Mellor S.K., Kavaliers M., and Ossenkopp K.-P. The effects of lipopolysaccharide and lithium chloride on the ingestion of a bitter-sweet taste: comparing intake and palatability. Brain Behav. Immun. 19 (2005) 564-573
14. Cross-Mellor S.K., Kent W.D.T., Kavaliers M., and Ossenkopp K.-P. Examining the effects of lipopolysaccharide and cholecystokinin on water ingestion: comparing intake and palatability. Brain Res. 861 (2000) 220-232
15. Cross-Mellor S.K., Kent W.D.T., Ossenkopp K.-P., and Kavaliers M. Differential effects of lipopolysaccharide and cholecystokinin on sucrose intake and palatability. Am. J. Physiol. 277 (1999) R705-R715
16. Cross-Mellor S.K., Roberts S., Kavaliers M., and Ossenkopp K.-P. Activation of the immune system in rats with lipopolysaccharide reduces voluntary sucrose intake but not intraoral intake. Pharmacol. Biochem. Behav. 76 (2003) 153-159
17. Cunningham A.J., Murray C.A., O'Neill L.A., Lynch M.A., and O'Connor J.J. Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. Neurosci Lett. 203 (1996) 17-20
18. Cunningham C., and Sanderson D.J. Malaise in the water maze: untangling the effects of LPS and IL-1beta on learning and memory. Brain Behav. Immun. 22 (2008) 1117-1127
19. Dantzer R. Innate immunity at the forefront of psychoneuroimmunology. Brain Behav. Immun. 18 (2004) 1-6
20. Dinarello C.A. Interleukin-1 and the pathogenesis of the acute-phase response. N. Engl. J. Med. 311 (1984) 1413-1418
21. Domjan M., and Best M.R. Paradoxical effects of proximal unconditioned stimulus preexposure: interference with and conditioning of a taste aversion. J. Exp. Psychol. Anim. Behav. Process 3 (1977) 310-321
22. Eckel L.A., and Ossenkopp K.-P. Area postrema mediates the formation of rapid, conditioned palatability shifts in lithium-treated rats. Behav. Neurosci. 110 (1996) 202-212
23. Engeland C.G., Kavaliers M., and Ossenkopp K.-P. Sex differences in the effects of muramyl dipeptide and lipopolysaccharide on locomotor activity and the development of behavioral tolerance in rats. Pharmacol. Biochem. Behav. 74 (2003) 433-447
24. Engeland C.G., Kavaliers M., and Ossenkopp K.-P. Influence of the estrous cycle on tolerance development to LPS-induced sickness behaviors in rats. Psychoneuroendocrinology 31 (2006) 510-525
25. Franklin A.E., Engeland C.G., Kavaliers M., and Ossenkopp K.-P. Lipopolysaccharide-induced hypoactivity and behavioral tolerance development are modulated by the light-dark cycle in male and female rats. Psychopharmacology (Berl) 170 (2003) 399-408
26. Franklin A.E., Engeland C.G., Kavaliers M., and Ossenkopp K.-P. The rate of behavioral tolerance development to repeated lipopolysaccharide treatments depends upon the time of injection during the light-dark cycle: a multivariable examination of locomotor activity. Behav. Brain Res. 180 (2007) 161-173
27. Gahtan E., and Overmier J.B. Performance more than working memory disrupted by acute systemic inflammation in rats in appetitive tasks. Physiol. Behav. 73 (2001) 201-210
28. Gibertini M., Newton C., Friedman H., and Klein T.W. Spatial learning impairment in mice infected with Legionella pneumophila or administered exogenous interleukin-1-beta. Brain Behav. Immun. 9 (1995) 113-128
29. Grill H.J., and Norgren R. The taste reactivity test I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res. 143 (1978) 263-279
30. Grill H.J., and Norgren R. The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats. Brain Res. 143 (1978) 281-297
31. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 12 (1988) 123-137
32. Hennigan A., Trotter C., and Kelly A.M. Lipopolysaccharide impairs long-term potentiation and recognition memory and increases p75NTR expression in the rat dentate gyrus. Brain Res. 1130 (2007) 158-166
33. Hua F., Ma J., Ha T., Xia Y., Kelley J., Williams D.L., Kao R.L., Browder I.W., Schweitzer J.B., Kalbfleisch J.H., and Li C. Activation of Toll-like receptor 4 signaling contributes to hippocampal neuronal death following global cerebral ischemia/reperfusion. J. Neuroimmunol. 190 (2007) 101-111
34. Kent W.D.T., Cross-Mellor S.K., Kavaliers M., and Ossenkopp K.-P. Acute effects of corticosterone on LiCl-induced rapid gustatory conditioning in rats: a taste reactivity analysis. NeuroReport 11 (2000) 3903-3908
35. Kent W.D.T., Cross-Mellor S.K., Kavaliers M., and Ossenkopp K.P. Acute effects of corticosterone on LiCl-induced rapid gustatory conditioning in rats: a microstructural analysis of licking patterns. Behav. Brain Res. 136 (2002) 143-150
36. Kohman R.A., Tarr A.J., Byler S.L., and Boehm G.W. Age increases vulnerability to bacterial endotoxin-induced behavioral decrements. Physiol. Behav. 91 (2007) 561-565
37. Larson S.J. Behavioral and motivational effects of immune-system activation. J. Gen. Psychol. 129 (2002) 401-414
38. Loy I., and Hall G. Taste aversion after ingestion of lithium chloride: an associative analysis. Q. J. Exp. Psychol. B 55 (2002) 365-380
39. Moriez R., Salvador-Cartier C., Theodorou V., Fioramonti J., Eutamene H., and Bueno L. Myosin light chain kinase is involved in lipopolysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. Am. J. Pathol. 167 (2005) 1071-1079
40. Nakano K., Suzuki S., and Oh C. Significance of increased secretion of glucocorticoids in mice and rats injected with bacterial endotoxin. Brain Behav. Immun. 1 (1987) 159-172
41. O'Dwyer S.T., Michie H.R., Ziegler T.R., Revhaug A., Smith R.J., and Wilmore D.W. A single dose of endotoxin increases intestinal permeability in healthy humans. Arch. Surg. 123 (1988) 1459-1464
42. Oitzl M.S., van Oers H., Schobitz B., and de Kloet E.R. Interleukin-1 beta, but not interleukin-6, impairs spatial navigation learning. Brain Res. 613 (1993) 160-163
43. Ossenkopp K.-P., and Eckel L.A. Toxin-induced conditioned changes in taste reactivity and the role of the chemosensitive area postrema. Neurosci. Biobehav. Rev. 19 (1995) 99-108
44. Ossenkopp K.-P., Kent W.D.T., and Clarke S.N.D.A. Tracking rapid palatability shifts in rats ingesting toxin containing fluids. Int. Behav. Neurosci. Soc. Abstr. 6 (1997) 36
45. Ossenkopp K.-P., Ladowsky R.L., and Eckel L.A. Forced-choice discrimination of equimolar NaCl and LiCl solutions in rats: effects of ablating the chemosensitive area postrema on acquisition and retention. Behav. Brain Res. 87 (1997) 15-24
46. Paues J., Mackerlova L., and Blomqvist A. Expression of melanocortin-4 receptor by rat parabrachial neurons responsive to immune and aversive stimuli. Neuroscience 141 (2006) 287-297
47. Pugh C.R., Kumagawa K., Fleshner M., Watkins L.R., Maier S.F., and Rudy J.W. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain Behav. Immun. 12 (1998) 212-229
48. Pugh C.R., Fleshner M., Watkins L.R., Maier S.F., and Rudy J.W. The immune system and memory consolidation: a role for the cytokine IL-1beta. Neurosci. Biobehav. Rev. 25 (2001) 29-41
49. Riley A.L., and Tuck D.L. Conditioned food aversions: a bibliography. Ann. N.Y. Acad. Sci. 443 (1985) 381-437
50. Sakai N., and Yamamoto T. Possible routes of visceral information in the rat brain in formation of conditioned taste aversion. Neurosci. Res. 35 (1999) 53-61
51. Sandi C., and Rose S.P. Training-dependent biphasic effects of corticosterone in memory formation for a passive avoidance task in chicks. Psychopharmacology (Berl) 133 (1997) 152-160
52. Shaw K.N., Commins S., and O'Mara S.M. Lipopolysaccharide causes deficits in spatial learning in the watermaze but not in BDNF expression in the rat dentate gyrus. Behav. Brain Res. 124 (2001) 47-54
53. Song C., Phillips A.G., Leonard B.E., and Horrobin D.F. Ethyl-eicosapentaenoic acid ingestion prevents corticosterone-mediated memory impairment induced by central administration of interleukin-1beta in rats. Mol. Psychiatry 9 (2004) 630-638
54. Sparkman N.L., Buchanan J.B., Heyen J.R., Chen J., Beverly J.L., and Johnson R.W. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J. Neurosci. 26 (2006) 10709-10716
55. Sparkman N.L., Kohman R.A., Scott V.J., and Boehm G.W. Bacterial endotoxin-induced behavioral alterations in two variations of the Morris water maze. Physiol. Behav. 86 (2005) 244-251
56. Sparkman N.L., Kohman R.A., Scott V.J., and Boehm G.W. Bacterial endotoxin-induced behavioral alterations in two variations of the Morris water maze. Physiol. Behav. 86 (2005) 244-251
57. Spector A.C., Breslin P.A.S., and Grill H.J. Taste reactivity as a dependent measure of the rapid formation of conditioned taste aversion: a tool for the neural analysis of taste-visceral associations. Behav. Neurosci. 102 (1988) 942-952
58. Swiergiel A.H., and Dunn A.J. Feeding, exploratory, anxiety- and depression-related behaviors are not altered in interleukin-6-deficient male mice. Behav. Brain Res. 171 (2006) 94-108
59. Swiergiel A.H., Smagin G.N., and Dunn A.J. Influenza virus infection of mice induces anorexia: comparison with endotoxin and interleukin-1 and the effects of indomethacin. Pharmacol. Biochem. Behav. 57 (1997) 389-396
60. Tanaka S., Ide M., Shibutani T., Ohtaki H., Numazawa S., Shioda S., and Yoshida T. Lipopolysaccharide-induced microglial activation induces learning and memory deficits without neuronal cell death in rats. J. Neurosci. Res. 83 (2006) 557-566
61. Tenk C.M., Kavaliers M., and Ossenkopp K.P. The effects of acute corticosterone on lithium chloride-induced conditioned place aversion and locomotor activity in rats. Life Sci. 79 (2006) 1069-1080
62. Thomson L.M., and Sutherland R.J. Systemic administration of lipopolysaccharide and interleukin-1beta have different effects on memory consolidation. Brain Res. Bull. 67 (2005) 24-29
63. Thomson L.M., and Sutherland R.J. Interleukin-1beta induces anorexia but not spatial learning and memory deficits in the rat. Behav. Brain Res. 170 (2006) 302-307
64. Yirmiya R., Winocur G., and Goshen I. Brain interleukin-1 is involved in spatial memory and passive avoidance conditioning. Neurobiol. Learn. Mem. 78 (2002) 379-389
65. Young E.E., Baumbauer K.M., Elliot A., and Joynes R.L. Lipopolysaccharide induces a spinal learning deficit that is blocked by IL-1 receptor antagonism. Brain Behav. Immun. 21 (2007) 748-757