Differential effects of neurokinin-1 receptor activation in subregions of the periaqueductal gray matter on conditional and unconditional fear behaviors in rats

Behavioral Neuroscience

Volumn 112, Issue 5, 1998, Pages 1125-1135

  Mongeau, Raymond ^b   De Oca, Beatrice M ^a,c   Fanselow, Michael S ^a,c   Marsden, Charles A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c California Institute of Technology HHMI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINOVALERYLSUBSTANCE P [7-11][9 PROLINE 10 (N METHYLLEUCINE)]; NEUROKININ 1 RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVERSIVE BEHAVIOR; CONTROLLED STUDY; FEAR; FREEZING; MALE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; RAT; SHOCK; TAIL FLICK TEST;

EID: 3643093657     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.112.5.1125     Document Type: Article

References (62)

1. Aguiar, M. S., & Brandao, M. L. (1994). Conditioned place aversion produced by microinjections of substance P into the periaqueductal gray of rats. Behavioural Pharmacology, 5, 369-373.
2. Aguiar, M. S., & Brandao, M. L. (1996). Effects of microinjections of the neuropeptide substance Pin the dorsal periaqueductal gray on the behaviour of rats in the plus-maze test. Physiology and Behavior, 60, 1183-1186.
3. A receptors in the midbrain central grey mediate the antiaversive action of GABA. European Journal of Pharmacology. 135, 225-229.
4. Beattie, D. T., Beresford, I. J. M., Connor, H. E., Marshall, F. H., Hawcock, A. B., Hagan, R. M., Bowers, J., Birch, P. J., & Ward, P. (1995). The pharmacology of GR203040, a novel, potent and selective non-peptide tachykinin NK1 receptor antagonist. British Journal of Pharmacology, 116, 3149-3157.
5. Beckett, S., & Marsden, C. A. (1995). Computer analysis and quantification of periaqueductal grey-induced defence behaviour. Journal of Neuroscience Methods, 58, 157-161.
6. 1A receptors inhibits midbrain periaqueductal gray neurons of the rat. Brain Research, 612, 56-60.
7. Bolles, R. C., & Fanselow, M. S. (1980). A perceptual-defensive-recuperative model of fear and pain. Behavioural Brain Research, 3, 291-301.
8. Brandao, M. L., Coimbra, N. C., & Borges, P. C. (1990). Effects of morphine and midazolam on reactivity to peripheral noxious and central aversive stimuli. Neuroscience Biobehavioral Review, 14, 495-499.
9. Brodin, E., Rosen, A., Schott, E., & Brodin, K. (1994). Effects of sequential removal of rats from a group cage, and of individual housing of rats, on substance P, cholecystokinin and somatostatin levels in the periaqueductal grey and limbic regions. Neuropeptides, 26, 253-260.
10. Burdin, T. A., Graeff, F. G., & Pela, I. R. (1992). Opioid mediation of the antiaversive and hyperalgesic actions of bradykinin injected into the dorsal periaqueductal gray of the rat. Physiology and Behavior, 52, 405-410.
11. Culman, J., Tschope, C., Jost, N., Itoi, K., & Unger, T. H. (1993). Substance P and neurokinin A induced desensitization to cardiovascular and behavioral effects: Evidence for the involvement of different tachykinin receptors. Brain Research, 625, 75-83.
12. Cumberbatch, M. J., Chizh, B. A., & Headley, P. M. (1995). Modulation of excitatory amino acid responses by tachykinins and selective tachykinin receptor agonists in the rat spinal cord. British Journal of Pharmacology, 115, 1005-1012.
13. 11]- substance P. Brain Research, 531, 333-337.
14. Deakin, J. F., Graeff, F. G., & Guimaraes, F. (1992). 5-HT receptor subtypes and the modulation of aversion. In C. Marsden & D. J. Heal (Eds.), Central serotonin receptors and psychotropic drugs (pp. 147-174). Oxford, England: Blackwell Scientific Publications.
15. Depaulis, A., & Bandler, R. (1991). The midbrain periaqueductal gray matter: Functional anatomical and neurochemical organization. New York: Plenum.
16. Di Scala, G., Mana, M. J., Jacobs, W. J., & Phillips, A. G. (1987). Evidence of Pavlovian conditioned fear following electrical stimulation of the periaqueductal grey in the rat. Physiology and Behavior, 40, 55-63.
17. Eide, P. K., & Hole, K. (1991). Interactions between serotonin and substance P in the spinal regulation of nociception. Brain Research, 550, 225-230.
18. 7, is not state dependent: Implication of substance P in aversion. Experimental Brain Research, 73, 354-356.
19. Elliot, P. J., & Iversen, S. D. (1986). Behavioural effects of tachykinins and related peptides. Brain Research, 381, 68-76.
20. Fanselow, M. S. (1980). Conditional and unconditional components of post-shock freezing. Pavlovian Journal of Biological Sciences, 15, 177-182.
21. Fanselow, M. S. (1986). Associative vs topographical accounts of the immediate shock-deficit in rats: Implications for the response selection rules governing species-specific defensive reactions. Learning and Motivation, 17, 16-39.
22. Fanselow, M. S., DeCola, J. P., De Oca, B. M., & Landeira-Fernandez, J. (1995). Ventral and dorsolateral regions of the midbrain periaqueductal gray (PAG) control different stages of defensive behavior: Dorsolateral PAG lesions enhance the defensive freezing produced by massed and immediate shock. Aggressive Behavior, 21, 63-77.
23. Gradin, K., & Persson, B. (1992). Cardiovascular effects of intrathecal administration of substance P in the rat: Interaction with serotonergic mechanisms. Journal of Neural Transmission, 87, 199-213.
24. Graeff, F. G., Silveira, M. C., Nogueira, R. L., Audi, E. A., & Oliveira, R. M. (1993). Role of the amygdala and periaqueductal gray in anxiety and panic. Behavioural Brain Research, 58, 123-131.
25. Grant, F. L., Balfour, D. J. K., & Beresford, I. J. M. (1994, December). Effects of intra-dorsal raphe injections of NK1 receptor ligands on locomotor and freezing behaviour and 5-HT overflow in the ventral hippocampus of the rat. British Journal of Pharmacology, 113 (12Suppl.), 153.
26. Hagan, R. M., Ireland, S. J., Jordan, C. C., Beresford, I. J., Deal, M. J., & Ward, P. (1991). Receptor-selective, peptidase-resistant agonists at neurokinin NK-1 and NK-2 receptors: New tools for investigating neurokinin function. Neuropeptides, 19, 127-135.
27. Hammer, G. D., & Kapp, B. S. (1986). The effects of naloxone administered into the periaqueductal gray on shock-elicited freezing behavior in the rat. Behavioral and Neural Biology, 46, 189-195.
28. Henry, J. L., Krnjevic, K., & Morris, M. E. (1975). Substance P and spinal neurones. Canadian Journal of Physiology and Pharmacology, 53, 423-432.
29. LeDoux, J. E. (1995). Emotion: Clues from the brain. Annual Review of Psychology, 46, 209-235.
30. Li, Y. Q., Jia, H. G., Rao, Z. R., & Shi, J. W. (1990). Serotonin-, substance P- or leucine-enkephalin-containing neurons in the midbrain periaqueductal gray and nucleus raphe dorsalis send projection fibers to the central amygdaloid nucleus in the rat. Neuroscience Letters, 120, 124-127.
31. Li, Y. Q., Zeng, S. L., Dong, Y. X., Rao, Z. R., & Shi, J. W. (1991). Serotonin-, substance P- and tyrosine hydroxylase-like immuno-reactive neurons projecting from the periaqueductal gray to the ventromedial hypothalamic nucleus in the rat. Neuroscience Letters, 134, 33-36.
32. Li, Y. Q., Zeng, S. L., Rao, Z. R., & Shi, J. W. (1992). Serotonin-, substance P- and tyrosine hydroxylase-like immunoreactive neurons projecting from the midbrain periaqueductal gray to the nucleus tractus solitarii in the rat. Neuroscience Letters, 134, 175-179.
33. Liebman, J. M., Mayer, D. J., & Liebeskin, J. C. (1970). Mesencephalic central gray lesions and fear-motivated behavior in rats. Brain Research, 23, 353-370.
34. Liu, R. P., & Swenberg, M. L. (1988). Autoradiographic localization of substance P ligand binding sites and distribution of immunoreactive neurons in the periaqueductal gray of the rat. Brain Research, 475, 73-79.
35. Maeno, H., Kiyama, H., & Tohyama, M. (1993). Distribution of the substance P receptor (NK-1 receptor) in the central nervous system. Molecular Brain Research, 18, 43-58.
36. Magoul, R., Onteniente, B., Oblin, A., & Calas, A. (1986). Inter-and intracellular relationship of substance P-containing neurons with serotonin and GABA in the dorsal raphe nucleus: Combination of autoradiographic and immunocytochemical techniques. Journal of Histochemistry and Cytochemistry, 34, 735-742.
37. Maier, S. F., Busch, C. R., Maswood, S., Grahn, R. E., & Watkins, L. R. (1995). The dorsal raphe nucleus is a site of action mediating the behavioral effects of the benzodiazepine receptor inverse agonist DMCM. Behavioral Neuroscience, 109, 759-766.
38. Maier, S. F., Grahn, R. E., Maswood, S., & Watkins, L. R. (1995). The benzodiazepine receptor antagonists flumazenil and CGS8216 block the enhancement of fear conditioning and interference with escape behavior produced by inescapable shock. Psychopharmacology, 121, 250-258.
39. Malick, J. B., & Goldstein, J. M. (1978). Analgesic activity of substance P following intracerebral administration in rats. Life Sciences, 23, 835-844.
40. Mason, G. S., & Elliot, P. J. (1992). Behavioural consequences following infusion of selective neurokinin agonists into the median raphe nucleus of the rat. Neuropharmacology, 31, 757-760.
41. Mongeau, R., & Marsden, C. A. (1997a). Effect of central and peripheral administrations of cholecystokinin-tetrapeptide on panic-like reactions induced by stimulation of the dorsal periaqueductal grey area in the rat. Biological Psychiatry, 42, 335-344.
42. 1A-receptor-mediated inhibition of panic-like behaviours in rats. Psychopharmacology, 131, 321-328.
43. Moss, M. S., & Basbaum, A. I. (1983). The peptidergic organization of the cat periaqueductal gray: II. The distribution of immunoreactive substance P and vasoactive intestinal polypeptide. Journal of Neuroscience, 3, 1437-1449.
44. Neckers, L. M., Schwartz, J. P., Wyatt, R. J., & Speciale, S. G. (1979). Substance P afferents from the habenula innervate the dorsal raphe nucleus. Experimental Brain Research, 37, 619-623.
45. Paris, J. M., & Lorens, S. A. (1989). A dose-response analysis of intra-raphe tachykinin-induced hyperactivity. Journal of Pharmacology and Experimental Therapeutics, 251, 388-393.
46. Paxinos, A., & Watson, C. (1986). The rat brain in stereotaxic coordinates. New York: Academic Press.
47. Picard, P., Regoli, D., & Couture, R. (1994). Cardiovascular and behavioural effects of centrally administered tachykinins in the rat: Characterization of receptors with selective antagonists. British Journal of Pharmacology, 112, 240-249.
48. Przewlocka, B., Stala, L., Scheel-Kruger, J., & Przewlocki, R. (1986). Different behavioral responses of rats to kainate injections into the dorsal and median raphe nuclei. Polish Journal of Pharmacology and Pharmacy, 38, 509-519.
49. Quirion, R., Shults, C. W., Moody, T. W., Pert, C. B., Chase, T. N., & O'Donohue, T. L. (1983). Autoradiographic distribution of substance Preceptors in rat central nervous system. Nature, 303, 714-716.
50. Rizvi, T. A., Ennis, M., Behbehani, M. M., & Shipley, M. T. (1991). Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity. Journal of Comparative Neurology, 303, 121-131.
51. Rosen, A., Brodin, K., Eneroth, P., & Brodin, E. (1992). Short-term restraint stress and s.c. saline injection alter the tissue levels of substance P and cholecystokinin in the periaqueductal grey and limbic regions of rat brain. Acta Physiologica Scandinavica, 146, 341-348.
52. Rosen, A., Franck, J., & Brodin, E. (1995). Effects of acute systemic treatment with the 5 HT-uptake blocker alaproclate on tissue levels and release of substance P in rat periaqueductal grey. Neuropeptides, 28, 317-324.
53. Rupniak, N. M. J., Webb, J. K., Williams, A. R., Boyce, S., & Hill, R. G. (1995). Antinociceptive activity of the tachykinin NK1 receptor antagonist, CP-99,994, in conscious gerbils. British Journal of Pharmacology, 116, 1937-1943.
54. Russo, A. S., Guimaraes, F. S., De Aguiar, J. C., & Graeff, F. G. (1993). Role of benzodiazepine receptors located in the dorsal periaqueductal grey of rats in anxiety. Psychopharmacology, 110, 198-202.
55. Shaikh, M. B., Lu, C. L., & Siegel, A. (1991). Affective defense behavior elicited from the feline midbrain periqueductal gray is regulated by mu and delta opioid receptors. Brain Research, 557, 344-348.
56. Siegel, R. A., Duker, E.-M., Fuchs, E., Pahnke, U., & Wuttke, W. (1984). Responsiveness of mesolimbic, mesocortical, septal and hippocampal cholecystokinin and substance P neuronal systems to stress, in the male rat. Neurochemistry International, 6, 783-789.
57. Speciale, S. G., Neckers, L. M., & Wyatt, R. J. (1980). Habenular modulation of raphe indoleamine metabolism. Life Sciences, 27, 2367-2372.
58. Stezhka, V. V., & Lovick, T. A. (1994). Inhibitory and excitatory projections from the dorsal raphe nucleus to neurons in the dorsolateral periaqueductal gray matter in slices of midbrain maintained in vitro. Neuroscience, 62, 177-187.
59. Tallaksen-Greene, S. J., Eide, R., & Wessendorf, M. W. (1993). Regional distribution of serotonin and substance P co-existing in nerve fibers and terminals in the brainstem of the rat. Neuroscience, 53, 1127-1142.
60. Teixeras, R. M., Santos, A. R., Ribeiro, S. J., Calixto, J. B., Rae, G. A., & De Lima, T. C. (1996). Effects of central administration of tachykinin receptor agonists and antagonists on plus-maze behavior in mice. European Journal of Pharmacology, 311, 7-14.
61. Tershner, S. A., & Helmstetter, F. J. (1996). Injections of corticotropin-releasing factor into the periaqueductal gray enhance Pavlovian fear conditioning. Psychobiology, 24, 49-56.
62. Vincent, S. R., Staines, W. A., McGeer, E. G., & Fibiger, H. C. (1980). Transmitters contained in the efferent of the habenula. Brain Research, 195, 479-484.