Excitotoxic lesions of the tegmental pedunculopontine nucleus impair copulation in naive male rats and block the rewarding effects of copulation in experienced male rats

European Journal of Neuroscience

Volumn 18, Issue 9, 2003, Pages 2581-2591

  Kippin, Tod E ^a   Van Der Kooy, Derek ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Arousal; Erection; Exhaustion; Motivation; Partner preference; Sexual behaviour

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AVERSION; BRAIN INJURY; CONTROLLED STUDY; COPULATION; EJACULATION; FEMALE; MALE; NONHUMAN; PENIS ERECTION; PRIORITY JOURNAL; RAT; RAT STRAIN; REWARD; SEXUAL BEHAVIOR; TEGMENTUM;

ANIMALS; CONDITIONING, CLASSICAL; COPULATION; DIAZEPAM; EXCITATORY AMINO ACID AGONISTS; FEMALE; GABA MODULATORS; MALE; MORPHINE; N-METHYLASPARTATE; NARCOTICS; OVARIECTOMY; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; RATS; RATS, LONG-EVANS; REWARD; SEXUAL BEHAVIOR, ANIMAL;

EID: 0344874599     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02918.x     Document Type: Article

References (70)

1. Agmo, A. (2003a) Lack of opioid or dopaminergic effects on unconditioned sexual incentive motivation in male rats. Behav. Neurosci., 117, 55-68.
2. Agmo, A. (2003b) Unconditioned sexual incentive motivation in the male Norway rat (Rattus norvegicus). J. Comp. Psychol., 117, 3-14.
3. Agmo, A. & Berenfeld, R. (1990) Reinforcing properties of ejaculation in the male rat: the role of opioids and dopamine. Behav. Neurosci., 104, 177-182.
4. Agmo, A. & Gomez, M. (1993) Sexual reinforcement is blocked by infusion of naloxone into the medial preoptic area. Behav. Neurosci., 107, 812-818.
5. Alderson, H.L., Jenkins, T.A., Kozak, R., Latimer, M.P. & Winn, P. (2001) The effects of excitotoxic lesions of the pedunculopontine tegmental nucleus on conditioned place preference to 4%, 12%, and 20% sucrose solutions. Brain Res. Bull., 56, 599-605.
6. Bechara, A., Harrinton, F., Nader, K. & van der Kooy, D. (1992) Neurobiology of motivation: double dissociation of two motivational mechanisms mediating opiate reward in drug-naive versus drug-dependent animals. Behav. Neurosci., 106, 798-807.
7. Bechara, A., Nader, K. & van der Kooy, D. (1995) Neurobiology of withdrawal motivation: evidence for two separate aversive effects produced in morphine-naive versus morphine-dependent rats by both naloxone and spontaneous withdrawal. Behav. Neurosci., 109, 91-105.
8. Bechara, A. & van der Kooy, D. (1989) The tegmental pedunculopontine nucleus: a brainstem output of the limbic system is critical for the conditioned place preference produced by morphine and amphetamine. J. Neurosci., 9, 3400-3409.
9. Bechara, A. & van der Kooy, D. (1992a) A single brain stem substrate mediates the motivational effects of both opiates and food in non-deprived, but not deprived animals. Behav. Neurosci., 106, 351-363.
10. Bechara, A. & van der Kooy, D. (1992b) Lesions to the tegmental pedunculopontine nucleus: effects of locomotor activity induced by morphine and amphetamine. Pharmacol. Biochem. Behav., 42, 9-18.
11. Bespalov, A.Y., Tokarz, M.E., Bowen, S.E., Balster, R.L. & Beardsley, P.M. (1999) Effects of test conditions on the outcome of place conditioning with morphine and naltrexone in mice. Psychopharmacology, 141, 118-122.
12. Dai, S., Corrigall, W.A., Coen, K.M. & Kalant, H. (1989) Heroin self-administration by rats: influence of dose and physical dependence. Pharmacol. Biochem. Behav., 32, 1009-1015.
13. Di Chiara, G., Acquas, E., Tanda, G. & Cadoni, C. (1993) Drugs of abuse: biochemical surrogates of specific aspects of natural rewards? Biochem. Soc. Symp., 59, 65-81.
14. Dockstader, C.L. & van der Kooy, D. (2001) Mouse strain differences in opiate reward learning are explained by differences in anxiety, not reward or learning. J. Neurosci., 15, 9077-9081.
15. Everitt, B.J. (1990) Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci. Biobehav. Rev., 14, 217-232.
16. Fewell, G.D. & Meredith, M. (2002) Experience facilitates vomeronasal and olfactory influence on Fos expression in medial preoptic area during pheromone exposure or mating in male hamsters. Brain Res., 941, 91-106.
17. van Furth, W.R. & van Ree, J.M. (1996) Sexual motivation: involvement of endogenous opioids in the ventral tegmental area. Brain Res., 729, 20-28.
18. van Furth, W.R., Wolternik, G. & van Ree, J.M. (1995) Regulation of masculine sexual behavior: involvement of brain opioids and dopamine. Brain Res. Rev., 21, 162-184.
19. Hellemans, K.G., Shaham, Y. & Olmstead, M.C. (2002) Effects of acute and prolonged opiate abstinence on extinction behaviour in rats. Can. J. Exp. Psychol., 56, 241-252.
20. Hughes, A.M., Everitt, B.J. & Hubert, J. (1990) Comparative effects of preoptic area infusions of opioid peptides, lesions, and castration on sexual behavior in rats: studies of instrumental behavior, conditioned place preference, and partner preference. Psychopharmology, 102, 243-256.
21. Hutcheson, D.M., Everitt, B.J., Robbins, T.W. & Dickinson, A. (2001) The role of withdrawal in heroin addiction: enhances reward or promotes avoidance? Nature Neurosci., 4, 943-947.
22. Inglis, W.L., Dunbar, J.S. & Winn, P. (1994) Outflow from the nucleus accumbens to the pedunculopontine tegmental nucleus: a dissociation between locomotor activity and acquisition of responding for conditioned reinforcement stimulated by D-amphetamine. Neuroscience, 62, 51-64.
23. Keating, G.L., Walker, S.C. & Winn, P. (2002) An examination of the effects of bilateral excitotoxic lesions of the pendunculopontine tegmental nucleus on responding to sucrose reward. Behav. Brain Res., 134, 217-228.
24. Kim, J.A., Siegel, S. & Patenall, V.R. (1999) Drug-onset cues as signals: intraadministration associations and tolerance. J. Exp. Psychol. Anim. Behav. Process., 25, 491-504.
25. Kippin, T.E., Samaha, A.N., Sotiropoulos, V. & Pfaus, J.G. (2001) The development of olfactory conditioned ejaculatory preferences in the male rat. II. Parametric manipulation of conditioning session number and duration. Physiol. Behav., 73, 471-485.
26. Kippin, T.E., Talianakis, S., Schattmann, L., Bartholomew, S. & Pfaus, J.G. (1998) Olfactory conditioning of sexual behavior and mate selection in the male rat. J. Comp. Psychol., 112, 389-399.
27. Laviolette, S.R., Alexson, T.A. & van der Kooy, D. (2002) Lesions of the tegmental pedunculopontine nucleus switch the motivational valence of nicotine in the ventral tegmental area from rewarding to aversive. J. Neurosci., 22, 8653-8660.
28. Leri, F. & Franklin, K.B.J. (1998) Learning impairments caused by lesions to the pedunculopontine tegmental nucleus: an artifact of anxiety? Brain Res., 807, 187-192.
29. Leri, F. & Franklin, K.B.J. (2000) Diazepam modifies the effect of pedunculopontine lesions on morphine but not on amphetamine conditioned place preference. Behav. Brain Res., 117, 21-37.
30. Lopez, H.H. & Ettenberg, A. (2002) Exposure to female rats produces differences in c-fos induction between sexually-naive and experienced male rats. Brain Res., 947, 57-66.
31. McClintock, M.K. (1984) Group mating in the domestic rat as a context for sexual selection: consequences for the analysis of sexual behavior and neuroendocrine responses. Adv. Study. Behav., 14, 1-50.
32. McClintock, M.K., Anisko, J.J. & Adler, N.T. (1982) Group mating among Norway rats. II. The social dynamics of copulation: competition, cooperation, and mate choice. Anim. Behav., 30, 410-425.
33. Mehrara, B.J. & Baum, M.J. (1990) Naloxone disrupts the expression but not the acquisition by male rats of a conditioned place preference response for an oestrous female. Pyschopharmacology, 101, 118-125.
34. Meisel, R.L. & Sachs, B.D. (1994) The physiology of male sexual behavior. In Knobil, E. & Neill, J.D. (Eds), The Physiology of Reproduction, 2nd edn, Vol. 2. Raven Press, New York, pp. 3-105.
35. Mendelson, S.D. & Pfaus, J.G. (1989) Level searching: a new assay of sexual motivation in the male rat. Physiol. Behav., 45, 337-341.
36. Miller, R.L. & Baum, M.J. (1987) Naloxone inhibits mating and conditioned placed preference for an oestrous female in male rats soon after castration. Pharmacol. Biochem. Behav., 26, 781-789.
37. Mitchell, J.B. & Gratton, A. (1991) Opioid modulation and sensitization of dopamine release elicited by sexually relevant stimuli: a high speed chronoamperometric study in freely behaving rats. Brain Res., 551, 20-27.
38. Mitchell. J.B. & Gratton, A. (1992) Mesolimbic dopamine release elicited by activation of the accessory olfactory system: a high speed chronoamperometric study. Neurosci. Lett., 40, 81-84.
39. Nader, K., Bechara, A., Roberts, D.C. & van der Kooy, D. (1994) Neuroleptics block high-but not low-dose heroin place preferences: further evidence for a two-system model of motivation. Behav. Neurosci., 108, 1128-1138.
40. Nader, K., Bechara, A. & van der Kooy, D. (1997) Neurobiological constraints on behavioral models of motivation. Annu. Rev. Psychol., 48, 85-114.
41. Nader, K. & van der Kooy, D. (1997) Deprivation state switches the neurobiological substrates mediating opiate reward in the ventral tegmental area. J. Neurosci., 17, 383-390.
42. O'Hanlon, J.K. & Sachs, B.D. (1980) Penile reflexes in rats after different numbers of ejaculations. Behav. Neural Biol., 29, 338-348.
43. Olmstead, M.C. & Franklin, K.B.J. (1994a) Lesions of the pendunculopontine tegmental nucleus abolish catalepsy and locomotor depression induced by morphine. Brain Res., 662, 134-140.
44. Olmstead, M.C. & Franklin, K.B.J. (1994b) Lesions of the pedunculopontine tegmental nucleus block drug-induced reinforcement but not amphetamine-induced locomotion. Brain Res., 638, 29-35.
45. Olmstead, M.C., Inglis, W.L., Bordeaux, C.P., Clarke, E.J., Wallum, N.P., Everitt, B.J. & Robbins, T.W. (1999) Lesions of the pedunculopontine tegmental nucleus increase sucrose consumption but do not affect discrimination or contrast effects. Behav. Neurosci., 113, 732-743.
46. Olmstead, M.C., Munn, E.M., Franklin, K.B. & Wise, R.A. (1998) Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J. Neurosci., 18, 5035-5044.
47. Olmsted, M.C. & Franklin, K.B.J. (1993) Effects of pedunculopontine tegmental nucleus lesions on morphine-induced conditioned place preference and analgesia in the formalin test. Neuroscience, 57, 411-418.
48. Paredes, R.G. & Martinez, I. (2001) Naloxone blocks place preference conditioning after paced mating in female rats. Behav. Neurosci., 115, 1363-1367.
49. Parker, J.L. & van der Kooy, D. (1995) Tegmental pedunculopontine nucleus lesions do not block cocaine reward. Pharmacol. Biochem. Behav., 52, 77-83.
50. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego.
51. Pfaus, J.G. & Everitt, B.J. (1995) The psycholopharmacology of sexual behavior. In Bloom, F.E. & Kupfer, D.J. (Eds), Psychopharmacology, The Fourth Generation of Progress. Raven Press Ltd., New York, pp. 743-756.
52. Pfaus, J.G. & Gorzalka, B.B. (1987) Opiods and sexual behavior. Neurosci. Biobehav. Rev., 11, 1-34.
53. Pfaus, J.G., Kippin, T.E. & Centeno, S. (2001) Conditioning and sexual behavior: a review. Horm. Behav., 40, 291-321.
54. Podhorna, J. & Franklin, K.B.J. (1998) Lesions of the pedunculopontine tegmental nucleus increase anxiety in rats. Neuroreport, 9, 1783-1786.
55. Podhorna, J. & Franklin, K.B.J. (2000) Pontine tegmentum lesions increase anxiety-like behavior in rats: a comparison with anxiety produced by beta-CCE. Pharmacol. Biochem. Behav., 65, 267-273.
56. Rodriguez-Manzo, G. (1999) Yohimbine interacts with the dopaminergic system to reverse sexual satiation: further evidence for a role of sexual motivation in sexual exhaustion. Eur. J. Pharmacol., 372, 1-8.
57. Rodriguez-Manzo, G. & Fernandez-Guasti, A. (1995) Opioid antagonists and the sexual satiation phenomenon. Psychopharmacology, 133, 131-136.
58. Sachs, B.D. (1995) Context-sensitive variation in the regulation of erection. In Bancroft, J. (Ed.), The Pharmacology of Sexual Function and Dysfunction. Elsevier, Amsterdam, pp. 97-108.
59. Sachs, B.D. (1997) Erection evoked in male rats by airborne scent from estrous females. Physiol. Behav., 62, 921-924.
60. Sachs, B.D., Akasofu, K., Citron, J.H., Daniels, S.B. & Natoli, J.H. (1994) Noncontact stimulation from estrous females evokes penile erection in rats. Physiol. Behav., 55, 1073-1079.
61. Sachs, B.D. & Barfield, R.J. (1974) Copulatory behavior of male rats given intermittent electric shocks: theoretical implications. J. Comp. Physiol. Psychol., 86, 607-615.
62. Schroeder, B.E., Binzak, J.M. & Kelley, A.E. (2001) A common profile of prefrontal cortical activation following exposure to nicotine-or chocolate-associated contextual cues. Neuroscience, 105, 535-545.
63. Steckler, T., Inglis, W., Winn, P. & Sahgal, A. (1994) The pedunculopontine tegmental nucleus: a role in cognitive processes? Brain Res. Brain Res. Rev., 19, 298-318.
64. Stefurak, T.L. & van der Kooy, D. (1994) Tegmental pedunculopontine lesions in rats decrease saccharinís rewarding effects but not its memory-improving effects. Behav. Neurosci., 108, 972-980.
65. Szechtman, H., Hershkowitz, M. & Simatov, R. (1981) Sexual behavior decreases pain sensitivity and stimulates endogenous opioids in male rats. Eur. J. Pharm., 70, 279-285.
66. Taylor, S.A. & Dewsbury, D.A. (1990) Male preferences for females of different reproductive conditions: a critical review. In MacDonald, D.W., Muller-Schwarze, D. & Natynczuk, S.E. (Eds), Chemical Signals in Vertebrates 5. Oxford University Press, Oxford, pp. 184-198.
67. Wenkstern, D., Pfaus, J.G. & Fibiger, H.C. (1993) Dopamine transmission increases in the nucleus accumbens of male rats during their first exposure to sexually receptive female rats. Brain Res., 618, 41-46.
68. Whalen, R.E. (1961) Effects of mounting without intromission and intromission without ejaculation on sexual behavior and maze learning. J. Comp. Physiol. Psychol., 54, 409-415.
69. Winn, P., Brown, V.J. & Inglis, W.L. (1997) On the relationships between the striatum and the pedunculopontine tegmental nucleus. Rev. Neurobiol., 11, 241-261.
70. Wise, R.A. (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend., 51, 13-22.