Stress and re-stress increases conditioned taste aversion learning in rats: Possible frontal cortical and hippocampal muscarinic receptor involvement

European Journal of Pharmacology

Volumn 586, Issue 1-3, 2008, Pages 205-211

  Brand, Linda ^a   Groenewald, Ilse ^a   Stein, Dan J ^b   Wegener, Gregers ^c   Harvey, Brian H ^a  

^a NORTH WEST UNIVERSITY   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

Cholinergic; Conditioned taste aversion; Frontal cortex; Hippocampus; Muscarinic receptor; Posttraumatic stress disorder; Re stress; Single prolonged stress

Indexed keywords

MUSCARINIC RECEPTOR; QUINUCLIDINYL BENZILATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FRONTAL CORTEX; HIPPOCAMPUS; LEARNING; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; RECEPTOR DENSITY; SENSORY MEMORY; STRESS; TASTE AVERSION;

ANIMALS; AVOIDANCE LEARNING; HIPPOCAMPUS; LITHIUM CHLORIDE; MALE; MENTAL RECALL; MUSCARINIC ANTAGONISTS; PREFRONTAL CORTEX; QUINUCLIDINYL BENZILATE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M1; RECEPTORS, MUSCARINIC; STRESS DISORDERS, POST-TRAUMATIC; STRESS, PSYCHOLOGICAL; TASTE;

EID: 43549119009     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2008.03.004     Document Type: Article

References (77)

1. Acquas E., Wilson C., and Fibiger H.C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J. Neurosci. 16 (1996) 3089-3096
2. Adamec R.E. Partial kindling of the ventral hippocampus: identification of changes in limbic physiology which accompany changes in feline aggression and defense. Physiol. Behav. 49 (1991) 443-453
3. Adem A., Jolkkonen M., Bognanovic N., Islam A., and Karlsson E. Localization of M1 muscarinic receptors in rat brain using selective muscarinic toxin-1. Brain Res. Bull. 44 (1997) 597-601
4. American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-IV). 4th ed. Washington, D.C (1994)
5. Batsell W.R., and George J.W. Unconditioned stimulus intensity and retention interval effects. Physiol. Behav., 60 (1995) 1463-1467
6. Bermudez-Rattoni F., and McGaugh J.L. Insular cortex and amygdale lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion. Brain Res. 549 (1991) 165-170
7. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 72 (1976) 248-254
8. Bremner J.D., Vythilingam M., Vermetten E., Southwick S.M., McGlashan T., Nazeer A., Khan S., Vaccarino L.V., Soufer R., Garg K.P., Ng C.K., Staib L.H., Duncan J.S., and Charney D.S. MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. Am. J. Psychiatry 160 (2003) 924-932
9. Broersen L.M. Attentional processes and learning and memory in rats: the prefrontal cortex and hippocampus compared. Prog. Brain Res. 126 (2000) 79-94
10. Broersen L.M., Heinsbroek R.P.W., and De Bruin J.P.C. The role of the medial prefrontal cortex of rats in short term memory functioning: further support for the involvement of cholinergic rather than dopaminergic mechanisms. Brain Res. 674 (1995) 221-229
11. Buwalda B., Kole M.H.P., Veenema A.H., Huininga M., De Boer F.S., Korte M.S., and Koolhaas J.M. Long-term effects of social stress on brain and behavior: a focus on hipocampal functioning. Neurosci. Biobehav. Rev. 29 (2005) 83-97
12. Cahill L. The neurobiology of emotionally influenced memory. Implications for understanding traumatic memory. Ann. N. Y. Acad. Sci. 821 (1997) 238-246
13. Diorio D., Viau V., and Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamo-pituitary-adrenal responses to stress. J. Neurosci. 13 (1993) 3839-3847
14. Elzinga B.M., and Bremner J.D. Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)?. J. Affect. Disord. 70 (2002) 1-17
15. Everitt B.J., and Robbins T.W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48 (1997) 649-684
16. Fornari R.V., Moreira M.K., Gabriela M., and Oliveira M.G.M. Effects of the selective M1 muscarinic receptor antagonist dicyclomine on emotional memory. Learn. Mem. 7 (2000) 287-292
17. Garcia J., and Hankins W.G. On The Origin of Food Aversion Paradigms. In: Barker L.M., Best M.R., and Domjan M. (Eds). Learning Mechanisms in Food Selection (1977), Baylor University Press 3-19
18. Gilad G.M. The stress-induced response of the septohippocampal cholinergic system. A vectorial outcome of psychoneuroendocrinological interactions. Psychoneuroendocrinology 12 (1987) 167-184
19. Gonzalez A.M., and Pazos A. Modification of muscarinic acetylcholine receptors in the rat brain following chronic immobilization stress: an autoradiographic study. Eur. J. Pharmacol. 223 (1992) 25-31
20. Guitton J.M., and Dudai Y. Anxiety-like state associates with taste to produce conditioned taste aversion. Biol. Psychiatry 56 (2004) 901-904
21. Hackmann A., Ehlers A., Speckens A., and Clark D.M. Characteristics and content of intrusive memories in PTSD and their changes with treatment. J. Trauma Stress 17 (2004) 231-240
22. Harvey B.H., Brand L., Jeeva Z., and Stein D. Cortical/hippocampal monoamines, HPA-axis changes and aversive behavior following stress and restress in an animal model of post-traumatic stress disorder. Physiol. Behav. 87 (2006) 881-890
23. Harvey B.H., Naciti C., Brand L., and Stein D.J. Endocrine, cognitive and hippocampal/cortical 5HT1A/2A receptor changes evoked by a time-dependent sensitisation (TDS) stress model in rats. Brain Res. 983 (2003) 97-107
24. Harvey B.H., Naciti C., Brand L., and Stein D.J. Serotonin and stress: protective or malevolent actions in the biobehavioral response to repeated trauma. Ann. N. Y. Acad. Sci. 1032 (2004) 267-272
25. Herman J.P., and Cullinan W.E. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 20 (1997) 78-84
26. Hess C., and Blozovski D. Hippocampal muscarinic cholinergic mediation of spontaneous alternation and fear in the developing rat. Behav. Brain Res. 24 (1987) 203-214
27. Jacobson L., and Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr.Rev. 12 (1991) 118-134
28. Janowsky D.S., and Overstreet D.H. The role of acetylcholine mechanisms in affective disorders. Neuropsychopharmacology: The fifth generation of progress (2000), American college of neuropsychopharmacology 3-14
29. Kaufer D., Friedman A., Seidman S., and Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 393 (1998) 373-377
30. Khan S., and Liberzon I. Topiramate attenuates exaggerated acoustic startle in an animal model of posttraumatic stress disorder. Psychopharmacology 172 (2004) 225-229
31. Kohda K., Harada K., Kato K., Hoshino A., Motohashi J., Yamaji T., Morinobu S., Matsuoka N., and Kato N. Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model. Neuroscience 148 (2007) 22-23
32. Kopf S.R., Buchholzer M.L., Hilgert M., Loffelholz K., and Klein J. Glucose plus choline improve passive avoidance behaviour and increase hippocampal acetylcholine release in mice. Neuroscience 103 (2001) 365-371
33. Laborszky L., and Duque A. Local synaptic connections of basal forebrain neurons. Behav. Brain Res. 115 (2000) 143-158
34. Lamprea M.R., Cardenas F.P., Silveira R., Morato S., and Walsh T.J. Dissociation of memory and anxiety on a repeated elevated plus maze paradigm: forebrain cholinergic mechanisms. Behav. Brain Res. 117 (2000) 97-105
35. Liberzon I., Krstov M., and Young E.A. Stress-restress: effects on ACTH and fast feedback. Psychoneuroendocrinology 22 (1997) 443-453
36. Lopez J.F., Akil H., and Watson S.J. Neural circuits mediating stress. Biol. Psychiatry 46 (1999) 1461-1471
37. Lopez-Garcia J.C., Fernandez-Ruiz J., Escobar M.L., Bermudez-Rattoni F., and Tapia R. Effects of excitotoxic lesions of the nucleus basalis magnocellularis on conditioned taste aversion and inhibitory avoidance in the rat. Pharmacol. Biochem. Behav. 45 (1993) 147-152
38. Lydon R.G., and Nakajima S. Differential effects of scopolamine on working and reference memory depend upon level of training. Pharmacol. Biochem. Behav. 43 (1992) 645-650
39. Mark G.P., Rada P.V., and Shors T.J. Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala. Neuroscience 74 (1996) 767-774
40. McGaugh J.L. Memory: a century of consolidation. Science 287 (2000) 248-251
41. Mickley G.A., Kenmuir C.L., McMullen A.C., Yocom A.M., Valentine E.L., Dengler-Crish C.M., Weber B., Welman A.J., and Remmers-Roeber D.R. Dynamic processing of taste aversion extinction in the brain. Brain Res. 1016 (2004) 79-89
42. Miller K.E., and Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24 (2001) 167-202
43. Miranda M.I., Ferreira G., Ramirez-Lugo L., and Bermudez-Rattoni F. Role of cholinergic system on the construction of memories: taste memory encoding. Neurobiol. Learn. Mem. 80 (2003) 211-222
44. Morgan M.A., and Ledoux J.E. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav. Neurosci. 109 (1995) 681-688
45. Nachman M., and Ashe J.H. Learned taste aversions in rats as a function of dosage, concentration, and route of administration of LiCl. Physiol. Behav. 10 (1973) 73-78
46. Nachman M., Rauschenberger J., and Ashe J.H. Studies of learned aversions using non-gustatory stimuli. In: Barker L.M., Best M.R., and Domjan M. (Eds). Learning Mechanisms in Food Selection (1977), Baylor University Press 395-417
47. Nakajima S., and Masaki T. Taste aversion learning induced by forced swimming in rats. Physiol. Behav. 80 (2004) 623-628
48. Naor C., and Dudai Y. Transient impairment of cholinergic function in the rat insular cortex disrupts the encoding of taste in conditioned taste aversion. Behav. Brain Res. 79 (1996) 61-67
49. Newport J.D., and Nemeroff B.C. Neurobiology of posttraumatic stress disorder. Curr. Opin. Neurobiol. 10 (2000) 211-218
50. Pepeu G., and Giovannini G.M. Changes in acetylcholine extracellular levels during cognitive processes. Learn. Mem. 11 (2004) 21-27
51. Picciotto M.R., Alreja M., and Jentsch J.T. Acetylcholine. In: Davis K.L., Charney D., Coyle J.T., and Nemeroff C. (Eds). Neuropsychopharmacology: The fifth generation of progress (2002), American College of Neuropsychopharmacology 3-14
52. Purves D., Bonardi C., and Hall G. Enhancement of latent inhibition in rats with electrolytic lesions of the hippocampus. Behav. Neurosci. 109 (1995) 366-370
53. Ramirez-Lugo L., Miranda I., Escobar M.L., Espinosa E., Bermudez F., and Bermudez-Rattoni F. The role of cortical cholinergic pre- and post-synaptic receptors in taste memory formation. Neurobiol. Learn. Mem. 79 (2003) 184-193
54. Rau V., Decola J.P., and Fanselow M.S. Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder. Neurosci. Biobehav. Rev. 29 (2005) 1207-1223
55. 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
56. Ritter R., McGlone J.J., and Kelley K.W. Absence of lithium-induced taste aversion after area postrema lesion. Brain Res. 201 (1980) 501-506
57. Roth S.R., Schwartz M., and Teitelbaum P. Failure of recovered lateral hypothalamic rats to learn specific food aversions. J. Comp. Physiol. Psychol. 83 (1973) 184-197
58. Rozin P. The significance of learning mechanisms in food selection: some biology, psychology and sociology of science. In: Barker L.M., Best M.R., and Domjan M. (Eds). Learning Mechanisms in Food Selection (1977), Baylor University Press 557-589
59. Rozin P., and Kalat J.W. Specific hungers and poison avoidance as adaptive specializations of learning. Psychol. Rev. 78 (1971) 459-486
60. Sarter M., and Bruno J.P. Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencaphalic and brainstem afferents. Neuroscience 95 (2000) 933-952
61. Servatius R.S., Beck K.D., Moldow L.R., Salameh H., Tumminello T.P., and Short R.K. A stress-induced anxious state in male rats: corticotropin-releasing hormone induces persistent changes in associative learning and startle reactivity. Biol. Psychiatry 57 (2005) 865-872
62. Shin L.M., McNally R.J., Kosslyn S.M., Thompson W.L., Scott L.R., Alpert N.M., Metzger L.J., Lasko N.B., Orr S.P., and Pitman R.K. Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related posttraumatic stress disorder: a PET Investigation. Am. J. Psychiatry 156 (1999) 575-584
63. Shin L.M., Shin T.S., Heckers S., Krangel T., Macklin M.L., and Orr S.P. Explicit memory and hippocampal function in post traumatic stress disorder. Hippocampus 14 (2004) 292-300
64. Shors T.J., and Servatius R.J. The contribution of stressor intensity, duration, and context to the stress-induced facilitation of associative learning. Neurobiol. Learn. Mem. 68 (1997) 92-96
65. Smythe J.W., Murphy D., Bhatnagar S., Timothy C., and Costall B. The effects of intrahippocampal scopolamine infusions on anxiety in rats as measured by the black-white box test. Brain Res. Bulletin 45 (1998) 89-93
66. Stancampiano R., Cocco S., Cugusi C., Sarais L., and Fadda F. Serotonin and acetylcholine release response in the rat hippocampus during a spatial memory task. Neuroscience 89 (1999) 1135-1143
67. Stone M.F., Grimes B.S., and Katz D.B. Hippocampal inactivation enhances taste learning. Learn. Mem. 12 (2005) 579-586
68. Testa T.J., and Ternes J.W. Specificity of conditioning mechanisms in the modification of food. In: Barker L.M., Best M.R., and Domjan M. (Eds). Learning Mechanisms in Food Selection (1977), Baylor University Press 229-253
69. Van Der Zee E.A., and Luiten P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog. Neurobiol. 58 (1999) 409-471
70. Van Oyen Witvliet C. Traumatic intrusive imagery as an emotional memory phenomenon: a review of research and explanatory information processing theories. Clin. Psychol. Rev. 17 (1997) 509-536
71. Wegener G., Smith D.F., and Rosenberg R. 5-HT1A receptors in lithium-induced conditioned taste aversion. Psychopharmacology (Berl) 133 (1997) 51-54
72. Wegener G., Volke V., Bandpey Z., and Rosenberg R. Nitric oxide modulates lithium-induced conditioned taste aversion. Behav. Brain Res. 118 (2001) 195-200
73. Wenk G.L. The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol. Learn. Mem. 67 (1997) 85-95
74. Yehuda R., and Antelman S.M. Criteria for rationally evaluating animal models of posttraumatic stress disorder. Biol. Psychiatry 33 (1993) 479-486
75. Yamamoto T., Fujimoto Y., Shimura T., and Sakai N. Conditioned taste aversion in rats with excitotoxic brain lesions. Neurosci. Res. 22 (1995) 31-49
76. 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
77. Yamamura H.I., and Snyder S.H. Muscarinic cholinergic binding in rat brain. Proc. Natl. Acad. Sci. U S A 71 (1974) 1725-1729