Differential contributions of the basolateral and central nuclei of the amygdala in the negative affective component of chemical somatic and visceral pains in rats

European Journal of Neuroscience

Volumn 18, Issue 8, 2003, Pages 2343-2350

  Tanimoto, Sachi ^a   Nakagawa, Takayuki ^a   Yamauchi, Yosuke ^a   Minami, Masabumi ^a   Satoh, Masamichi ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Acetic acid; Conditioned place aversion; Excitotoxic lesion formalin; Sprague Dawley rats

Indexed keywords

ACETIC ACID; FORMALDEHYDE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVERSION; BASOLATERAL NUCLEUS; BEHAVIOR; BRAIN INJURY; BRAIN TOXICITY; CENTRAL NUCLEUS; CONDITIONING; CONTROLLED STUDY; MALE; MOOD DISORDER; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; REDUCTION; SENSATION; SOMATIC PAIN; STIMULUS; VISCERAL PAIN;

ACETIC ACID; AFFECT; AMYGDALA; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); ESCAPE REACTION; EXCITATORY AMINO ACID AGONISTS; FORMALDEHYDE; IBOTENIC ACID; MALE; PAIN; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; STAINING AND LABELING;

EID: 1642545200     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02952.x     Document Type: Article

References (67)

1. Bandler, R. & Shipley, M.T. (1994) Columnar organization in the midbrain periaqueductal gray: modules for emotional expression? Trends Neurosci., 17, 379-389.
2. Becerra, L., Breiter, H.C., Wise, R., Gonzalez, R.G. & Borsook, D. (2001) Reward circuitry activation by noxious thermal stimuli. Neuron, 32, 927-946.
3. Bernard, J.F. & Besson, J.M. (1990) The spino (trigemino) ponto-amygdaloid pathway: electrophysiological evidence for an involvement in pain process. J. Neurophysiol., 63, 473-490.
4. Bernard, J.F., Bester, H. & Besson, J.M. (1996) Involvement of the spino-parabrachio-amygdaloid and -hypothalamic pathways in the autonomic and affective emotional aspects of pain. Prog. Brain Res., 107, 243-255.
5. Bernard, J.F., Huang, G.F. & Besson, J.M. (1992) Nucleus centralis of the amygdala and the globus pallidus ventralis: electrophysiological evidence for an involvement in pain processes. J. Neurosci., 68, 551-569.
6. Bernard, J.F., Huang, G.F. & Besson, J.M. (1994) The parabrachial are: electrophysiological evidence for an involvement in visceral nociceptive processes. J. Neurophysiol., 71, 1646-1660.
7. Bornhövd, K., Quante, M., Glauche, V., Bromm, B., Weiller, C. & Büchel, C. (2002) Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. Brain, 125, 1326-1336.
8. Burstein, R. (1996) Somatosensory and visceral input to the hypothalamus and limbic system. Prog. Brain Res., 107, 257-267.
9. Bushnell, M.C., Duncan, G.H., Hofbauer, R.K., Ha, B., Chen, J.-I. & Carrier, B. (1999) Pain perception: is there a role for primary somatosensory cortex? Proc. Natl Acad. Sci. USA, 96, 7705-7709.
10. Carr, G.D., Fibiger, H.C. & Phillips, A.C. (1989) Conditioned place preference as a measure of drug reward. In Liebman, J.M. & Cooper, S.J. (Eds), The Neuropharmacological Basis of Reward. Oxford Science Publications, Oxford, pp. 254-319.
11. Clement, C.I., Keay, K.A., Podzebenko, K., Gordon, B.D. & Bandler, R. (2000) Spinal sources of noxious visceral and noxious deep somatic afferent drive onto the ventrolateral periaqueductal gray of the rat. J. Comp. Neurol., 425, 323-344.
12. Crown, E.D., King, T.E., Meagher, M.W. & Grau, J.W. (2000) Shock-induced hyperalgesia. III. Role of the bed nucleus of the stria terminalis and amygdaloid nuclei. Behav. Neurosci., 114, 561-573.
13. Davis, M. (1992) The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci., 104, 532-543.
14. Davis, M., Rainie, D. & Cassell, M. (1994) Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci., 17, 208-214.
15. Dayas, C.V., Buller, K.M., Crane, J.W., Xu, Y. & Day, T.A. (2001) Stressor categorization: acute physical and psychological stressors elicit distinctive recruitment patterns in the amygdala and in medullary noradrenergic cell groups. Eur. J. Neurosci., 14, 1143-1152.
16. Everitt, B.J., Cardinal, R.N., Hall, J., Parkinson, J.A. & Robbins, T.W. (2000) Differential involvement of amygdala subsystems in appetitive conditioning and drug addiction. In Aggleton, J.P., (Ed), The Amygdala: a Functional Analysis, 2nd edn. Oxford University Press Inc, New York, pp. 353-390.
17. Everitt, B.J., Morris, K.A., O'Brien, A. & Robbins, T.W. (1991) The basolateral amygdala-ventral striatal system and conditioned place preference: further evidence of limbic-striatal interactions underlying reward-related processes. Neuroscience, 42, 1-18.
18. Everitt, B.J., Parkinson, J.A., Olmstead, M.C., Arroyo, M., Robeldo, P. & Robbins, T.W. (1999) Associative processes in addiction and reward: The role of amygdala-ventral striatal subsystems. Ann. N.Y. Acad. Sci., 877, 412-438.
19. Frenois, F., Cador, M., Caillé, S., Stinus, L. & Moine, C.L. (2002) Neural correlates of the motivational and somatic components of naloxone-precipitated morphine withdrawal. Eur. J. Neurosci., 16, 1377-1389.
20. Gallagher, M. & Chiba, A.A. (1996) The amygdala and emotion. Curr. Opin. Neurobiol., 6, 221-227.
21. Gallagher, M., Graham, P.W. & Holland, P.C. (1990) The amygdala central nucleus and appetitive Pavlovian conditioning: lesions impair one class of conditioned behavior. J. Neurosci., 10, 1906-1911.
22. Gewirtz, J.C. & Davis, M. (1997) Second-order fear conditioning prevented by blocking NMDA receptors in amygdala. Nature, 388, 471-474.
23. Goldstein, L.E., Rasmusson, A.M., Bunney, B.S. & Roth, R.H. (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J. Neurosci., 16, 4787-4798.
24. Grijalva, C.V., Levin, E.D., Morgan, M., Roland, B. & Martin, F.C. (1990) Contrasting effects of centromedial and basolateral amygdaloid lesions on stress-related responses. Behav. Neurosci., 106, 518-528.
25. Hall, J., Parkinson, J.A., Connor, T.M., Dickinson, A. & Everitt, B.J. (2001) Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. Eur. J. Neurosci., 13, 1984-1992.
26. Hatfield, T., Han, J.-S., Conley, M., Gallagher, M. & Holland, P. (1996) Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects. J. Neurosci., 16, 5256-5265.
27. Helmstetter, F.J., Bellgowan, P.S.F. & Tershner, S.A. (1993) Modulation of spinal nociceptive reflexes by the microinjection of morphine into the amygdala. Neuroreport, 4, 471-474.
28. Helmstetter, F.J., Tershner, S.A., Poore, L.H. & Bellgowan, P.S.F. (1998) Antinociception following opioid stimulation of the basolateral amygdala is expressed through the periaqueductal gray and rostral ventromedial medulla. Brain Res., 779, 104-118.
29. Hiroi, N. & White, N.M. (1991) The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference. J. Neurosci., 11, 2107-2116.
30. Holahan, M.R. & White, N.M. (2002) Conditioned memory modulation, freezing, and avoidance as measures of amygdala-mediated conditioned fear. Neurobiol. Learn. Mem., 77, 250-275.
31. Jasmin, L., Burkey, A.R., Card, J.P. & Basbaum, A.I. (1997) Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-) parabrachio-amygdaloid, in the rat. J. Neurosci., 17, 3751-3765.
32. Johansen, J.P., Fields, H.L. & Manning, B.H. (2001) The affective component of pain in rodents: Direct evidence for a contribution of the anterior cingulate cortex. Proc. Natl Acad. Sci. USA, 98, 8077-8082.
33. Killcross, S., Robbins, T.W. & Everitt, B.J. (1997) Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature, 388, 377-380.
34. Koob, G.F. (1999) The role of the striatopallidal and extended amygdala systems in drug addiction. Ann. N.Y. Acad. Sci., 877, 445-460.
35. Kruzich, P.J. & See, R.E. (2001) Differential contributions of the basolateral and central amygdala in the acquisition and expression of conditioned relapse to cocaine-seeking behavior. J. Neurosci., 21, RC155 (1-5).
36. LaBuda, C.J. & Fuchs, P.N. (2000) A behavioral test paradigm to measure the aversive quality of inflammatory and neuropathic pain in rats. Exp. Neurol., 163, 490-494.
37. LeDoux, J.E. (1992) Brain mechanism of emotion and emotional learning. Curr. Opin. Neurobiol., 2, 191-197.
38. LeDoux, J.E., Cicchetti, P., Xagoraris, A. & Romanski, L.M. (1990) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J. Neurosci., 10, 1062-1069.
39. LeDoux, J.E., Iwata, J., Cicchetti, P. & Reis, D.J. (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci., 8, 2517-2529.
40. Lewis, T. (1942) Pain. Macmillan, New York.
41. Malzack, R. & Casey, K.L. (1968) Sensory, motivational, and central control, determinants of pain. In Kenshalo, D.R. (Ed), The skin senses. Thomas, Springfield IL, pp. 423-439.
42. Manning, B.H. (1998) A lateralized deficit in morphine antinociception after unilateral inactivation of the central amygdala. J. Neurosci., 18, 9453-9470.
43. McDonald, A.J., Mascagni, F. & Guo, L. (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience, 71, 55-75.
44. Menétrey, D., Gannon, A., Levine, J.D. & Basbaum, A.I. (1989) Expression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular and visceral stimulation. J. Comp. Neurol., 285, 177-195.
45. Merskey, H. & Bogduk, N. (1994) Classification of chronic pain: description of chronic pain syndromes and definition of pain terms. In Merskey, H. & Bogduk, N. (Eds), IASP Task Force on Taxonomy, 2nd Edn. IASP Press, Seattle.
46. Nakagawa, T., Katsuya, A., Tanimoto, S., Yamamoto, J., Yamauchi, Y., Minami, M. & Satoh, M. (2003) Differential patterns of c-fos mRNA expression in the amygdaloid nuclei induced by chemical somatic and visceral noxious stimuli in rats. Neurosci. Lett., 344, 197-200.
47. Neugebauer, V. & Li, W. (2002) Processing of nociceptive mechanical and thermal information in central amygdala neurons with knee-joint input. J. Neurophysiol., 87, 103-112.
48. Ottersen, O.P. (1982) Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J. Comp. Neurol., 205, 30-48.
49. Parkinson, J.A., Robbins, T.W. & Everitt, B.J. (2000) Dissociable roles of the central and basolateral amygdala in appetitive emotional learning. Eur. J. Neurosci., 12, 405-413.
50. Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th Edn. Academic Press, San Diego, CA.
51. Pitkänen, A., Savander, V. & LeDoux, J.E. (1997) Organization of intraamygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci., 20, 517-523.
52. Price, D.D. (2000) Psychological and neural mechanisms of the affective dimension of pain. Science, 288, 1769-1772.
53. Radulovic, J., Kammermeier, J. & Spiess, J. (1998) Relationship between Fos production and classical fear conditioning: effects of novelty, latent inhibition, and unconditioned stimulus preexposure. J. Neurosci., 18, 7452-7561.
54. Rainville, P., Ducan, G.H., Price, D.D., Carrier, B. & Bushnell, M.C. (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science, 277, 968-971.
55. Rodella, L., Rezzani, R., Gioia, M., Tredici, G. & Bianchi, R. (1998) Expression of Fos immunoreactivity in the rat supraspinal regions following noxious visceral stimulation. Brain Res. Bull., 47, 357-366.
56. Sewards, T.V. & Sewards, M.A. (2002) The medial pain system: Neural representations of the motivational aspect of pain. Brain Res. Bull., 59, 163-180.
57. Shi, C.-J. & Cassell, M.D. (1998) Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex. J. Comp. Neurol., 399, 469-491.
58. Shi, C.-J. & Davis, M. (1999) Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J. Neurosci., 19, 420-430.
59. Smith, Y., Paré, J.-F. & Paré, D. (2000) Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J. Comp. Neurol., 416, 496-508.
60. Swank, M.W. (1999) Coordinate regulation of Fos and Jun proteins in mouse brain by LiCl. Neuroreport, 10, 3685-3689.
61. Tzschentke, T.M. (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol., 56, 613-672.
62. Van Giersbergen, P.L.M., Palkovits, M. & De Jong, W. (1992) Involvement of neurotransmitters in the nucleus tractus solitarii in cardiovascular regulation. Physiol. Rev., 72, 789-824.
63. Walker, D.L., Toufexis, D.J. & Davis, M. (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol., 463, 199-216.
64. Watanabe, T., Yamamoto, R., Maeda, A., Nakagawa, T., Minami, M. & Satoh, M. (2002) Effects of excitotoxic lesions of the central or basolateral nucleus of the amygdala on naloxone-precipitated withdrawal-induced conditioned place aversion in morphine-dependent rats. Brain Res., 958, 423-428.
65. Werka, T. (1997) The effects of the medial and cortical amygdala lesions on post-stress analgesia in rats. Behav. Brain Res., 86, 59-65.
66. White, N.M. & McDonald, R.J. (2002) Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem., 77, 125-184.
67. Zubieta, J.K., Smith, Y.R., Bueller, J.A., Xu, Y., Kilbourn, M.R., Jewett, D.M., Meyer, C.R., Koeppe, R.A. & Stohler, C.S. (2001) Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science, 293, 311-315.