Skip to main content
SpringerLink
Log in

Comparative effects of preoptic area infusions of opioid peptides, lesions and castration on sexual behaviour in male rats: studies of instrumental behaviour, conditioned place preference and partner preference

  • Original Investigations
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

The effects on the sexual behaviour of male rats of excitotoxic amino acid-induced lesions of the medial preoptic area-anterior hypothalamic area (mPOA/AHA), infusions of β-endorphin, α-melanocyte stimulating hormone and naloxone into the mPOA/AHA, systemic naloxone and castration were compared using different behavioural paradigms. These included measures of unconditioned copulatory behaviour, instrumental responses for an oestrous female presented under a second-order schedule of reinforcement, conditioned place preference and partner preference. The results demonstrate that manipulations of the mPOA/AHA markedly affect consummatory aspects of sexual behaviour (mounting, intromitting and ejaculating) but tend not to affect appetitive or reward-related aspects of sexual behaviour, although intra-mPOA/AHA αMSH did result in a small increase in instrumental responses, while β-endorphin infused into the mPOA/AHA also abolished preference for an oestrous over an anoestrous female. Systemic naloxone, on the other hand, reduced instrumental behaviour and a place preference conditioned by prior sexual interaction, while the same compound infused into the mPOA/AHA markedly facilitated copulatory responses but did not affect other measures of appetitive sexual responses. Castration caused an extremely rapid attenuation of conditioned place preference which was apparent before the males had experienced reductions in their copulatory performance. This treatment only slowly reduced partner perference. The results indicate that the use of several behavioural procedures can reveal discrete actions of neuroendocrine treatments on separable psychological processes which underly the integrated pattern of masculine sexual behaviour. In particular, they suggest that the mPOA/AHA is especially concerned with the copulatory responses of mounting and intromitting, but is much less important for a variety of appetitive sexual acts as well as sexual reward, as measured in the place preference procedure. The marked effects of castration on conditioned place preference taken together with the lack of effect of lesions of the mPOA/AHA on this measure indicate that testosterone affects sexual reward-related processes by an action at a site other than the mPOA/AHA. The implications of these findings are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ågmo A, Berenfeld R (1990) Reinforcing properties of ejaculation in the male rat: The role of opioids and dopamine. Behav Neurosci 104:177–182

    Google Scholar 

  • Alderson LM, Baum MJ (1981) Differential effects of gonadal steroids on dopamine metabolism in mesolimbic and nigrostriatal pathways of male rat brain. Brain Res 218:189–206

    Google Scholar 

  • Bermant G, Davidson JM (1974) Biological bases of sexual behaviour. Harper and Row, New York

    Google Scholar 

  • Bitran D, Hull EM (1987) Pharmacological analysis of male rat sexual behaviour. Neurosci Biobehav Rev 11:365–389

    Google Scholar 

  • Bitran D, Hull EM, Holmes GM, Lokkingland KJ (1988) Regulation of male rat copulatory behaviour by preoptic incertohypothalamic dopamine neurons. Brain Res Bull 20:323–331

    Google Scholar 

  • Bozarth MA, Wise RA (1981) Heroin reward is dependent on a dopaminergic substrate. Life Sci 29:1881–1886

    Google Scholar 

  • Buggy J, Johnson AK (1977) Preoptic hypothalamic periventricular lesions: thirst deficits and hypernatremia. Am J Physiol 222:R44–52

    Google Scholar 

  • Cador M, Robbins TW, Everitt BJ (1989) Involvement of the amygdala in stimulus-reward associations: interactions with ventral striatum. Neuroscience 30:77–86

    Google Scholar 

  • Carr GD, Fibiger MC, Phillips AG (1989) Conditioned place preference as a measure of drug reward. In: Liebman JM, Cooper SJ (eds) Neuropharmacological basis of reward. Oxford University Press, Oxford

    Google Scholar 

  • Davidson JM (1966a) Activation of male rat's sexual behaviour by intracerebral implantation of androgen. Endocrinology 79:783–794

    Google Scholar 

  • Davidson JM (1966b) Characteristics of sex behaviour in male rats following castration. Anim Behav 14:266–272

    Google Scholar 

  • Edwards DA, Einhorn LC (1986) Preoptic and midbrain control of sexual motivation. Physiol Behav 37:329–335

    Google Scholar 

  • Everitt BJ (1990a) Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev 14:217–232

    Google Scholar 

  • Everitt BJ (1990b) Neuroendocrine and psychological mechanisms underlying masculine sexual behaviour. In: Archer T, Ahlenius S, Hansen S, Södersten P (eds) Biological psychology. Lawrence Erlbaum, New York (in press)

    Google Scholar 

  • Everitt BJ, Stacey P (1987) Studies of instrumental behaviour with sexual reinforcement in male rats(Rattus norvegicus): II. Effects of preoptic area lesions, castration and testosterone. J Comp Psychol 101:407–419

    Google Scholar 

  • Everitt BJ, Fray PJ, Kostarczyk E, Taylor S, Stacey P (1987) Studies of instrumental behaviour with sexual reinforcement in male rats(Rattus norvegicus): I. Control by brief visual stimuli paired with a receptive female. J Comp Psychol 101:395–406

    Google Scholar 

  • Everitt BJ, Cador M, Robbins TW (1989) Interactions between the amygdala and ventral striatum in stimulus-reward associations: studies using a second-order schedule of sexual reinforcement. Neuroscience 30:63–75

    Google Scholar 

  • Gaffan D, Harrison S (1987) Amygdalectomy and disconnection in visual learning for auditory secondary reinforcement by monkeys. J Neurosci 7:2285–2292

    Google Scholar 

  • Hansen S (1982) Hypothalamic control of motivation: the medial preoptic area and masculine sexual behaviour In: Sodersten P (ed) Behavioural neuroscience in scandinavia. Scand J Psychol [Suppl] 1:121–126

    Google Scholar 

  • Hansen S, Köhler C, Goldstein M, Steinbusch HWM (1982) Effects of ibotenic acid-induced neuronal degeneration in the medial preoptic area and lateral hypothalamic area on sexual behaviour in the male rat. Brain Res 239:213–232

    Google Scholar 

  • Hansen S, Drake af Hagelsrum LJK (1984) Emergence of displacement activities in the male rat following the thwarting of sexual behaviour. Behav Neurosci 98:868–883

    Google Scholar 

  • Hart BL (1974) Medial preoptic-anterior hypothalmic area and socio-sexual behaviour of male dogs: a comparative neuropsychological analysis. J Comp Physiol Psychol 86:328–349

    Google Scholar 

  • Hart BL (1986) Medial preoptic-anterior hypothalmic area and socio-sexual behaviour of male goats. Physiol Behav 36:301–305

    Google Scholar 

  • Hart BL, Voith VL (1978) Changes in urine spraying, feeding and sleep behaviour following medial preoptic-anterior hypothalamic lesions in cats. Brain Res 145:406–409

    Google Scholar 

  • Hart BL, Haugen CM, Peterson DM (1973) Effects of medial preoptic-anterior hypothalamic lesions on mating behaviour of male cats. Brain Res 54:177–191

    Google Scholar 

  • Hawkins CM, Everitt BJ, Herbert J (1989) The influence of steroid hormones on competing sexual and ingestive behavior in the male rat. Physiol Behav 44:291–300

    Google Scholar 

  • Heimer L, Larsson K (1966/7) Impairment of mating behaviour in male rats following lesions in the preoptic-anterior hypothalamic continuum. Brain Res 3:248–263

    Google Scholar 

  • Heimer L, Wilson RD (1975) The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the pyriform cortex and the neocortex. In: Santini M (ed) Golgi centennial symposium. Raven Press, New York, pp 177–192

    Google Scholar 

  • Hughes AM, Everitt BJ, Herbert J (1987) Selective effects of β-endorphin infused into the hypothalamus, preoptic area and bed nucleus of the stria terminalis on the sexual and ingestive behavour of male rats. Neuroscience 23:1063–1073

    Google Scholar 

  • Hughes AM, Everitt BJ, Herbert J (1988) The effects of simultaneous or separate infusions of some pro-opiomelanocortinderived peptides (β-endorphin, melanocyte stimulating hormone and corticotrophin-like intermediate polypeptide) and their acetylated derivatives upon sexual and ingestive behaviour of male rats. Neuroscience 27:689–698

    Google Scholar 

  • Hull EM, Bitran D, Pehek EA, Warner RK, Band LC, Holmes GM (1986) Dopaminergic control of male sex behaviour in rats: effects of an intracerebrally infused agonist. Brain Res 370:73–81

    Google Scholar 

  • Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus-reward association. Exp Neurol 36:362–377

    Google Scholar 

  • Kelley AE, Domesick VB, Nauta WJH (1982) The amygdala-striatal projection in the rat — an anatomical study by anterograde- and retrograde-tracing methods. Neuroscience 7:615–630

    Google Scholar 

  • Koob GF, Stinus L, Le Moal M, Bloom FE (1989) Opponent process theory of motivation: neurobiological evidence from studies of opiate dependence. Neurosci Biobehav Rev 13:135–140

    Google Scholar 

  • Lane (1981) A general analysis of variance program for microcomputers. Behav Res Meth Instrument 13:694

    Google Scholar 

  • Mehrara BJ, Baum MJ (1990) Naloxone disrupts the expression but not the acquisition by male rats of a conditioned place preference response for an oestrous female. Psychopharmacology (in press)

  • Merkx J (1984) Effect of castration and subsequent substitution with testosterone, dihydrotestosterone and oestradiol, on sexual preference behaviour in the male rat. Behav Brain Res 11:59–65

    Google Scholar 

  • Miller RL, Baum MJ (1987) Naloxone inhibits mating and conditioned place preference for an oestrous female in male rats soon after castration. Pharmacol Biochem Behav 26:781–789

    Google Scholar 

  • Mitchell JB, Stewart J (1990a) Sexual behavior in the male rat is facilitated by infusions of morphine and dynorphin into the ventral tegmental area, and by presentation of stimuli previously paired with injections of morphine. Pharmacol Biochem Behav (in press)

  • Mitchell JB, Stewart J (1990b) Facilitation of sexual behaviors in the male rat in the presence of stimuli previously paired with systemic injections of morphine. Pharmacol Biochem Behav (in press)

  • Mitchell JB, Stewart J (1990c) Facilitation of sexual behaviors in the male rat associated with intra-VTA injections of opiates. Pharmacol Biochem Behav (in press)

  • Mitchell JB Stewart J (1990d) Effects of castration, steroid replacement and sexual experience on mesolimbic dopamine and sexual behaviors in the male rat. Brain Research (in press)

  • Numan M, Smith HG (1984) Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav Neurosci 98:712–727

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, New York

    Google Scholar 

  • Pehek EA, Warner RK, Bazzett TJ, Bitran D, Band LC, Eaton RC, Hull EM (1988) Microinjection of cis-flupenthixol, a dopamine antagonist, into the medial preoptic area impairs sexual behaviour of male rats. Brain Res 443:70–76

    Google Scholar 

  • Pfaus JG, Gorzalka BB (1987) Opioids and sexual behavior. Neurosci Biobehav Rev 11:1–34

    Google Scholar 

  • Phillips AG, Fibiger HC (1985) Anatomical and neurochemical substrates of drug reward determined by conditioned place preference technique. In: Bozarth MA (ed) Methods of assessing the reinforcing properties of abused drugs. Springer, Berlin Heidelberg New York, pp 275–290

    Google Scholar 

  • Phillips AG, Le Piane FG (1980) Reinforcing effects of morphine microinjection into the ventral tegmental area. Pharmacol Biochem Behav 12:965–968

    Google Scholar 

  • Robbins TW, Cador M, Taylor JR, Everitt BJ (1989) Limbic-striatal interactions in reward-related processes. Neurosci Biobehav Rev 13:155–162

    Google Scholar 

  • Sachs BD (1978) Conceptual and neural mechanisms of masculine copulatory behaviour. In: McGill TE, Dewsbury DA, Sachs BD (eds) Sex and behaviour. Plenum Press, New York, pp 267–295

    Google Scholar 

  • Sachs BD, Barfield RJ (1976) Functional analysis of of masculine copulatory behaviour in the rat. In: Rosenblatt JS, Hinde RA, Shaw E, Beer C (eds) Advances in the study of behaviour; vol 7. Academic Press, Orlando, Florida, pp 91–154

    Google Scholar 

  • Sachs BD, Meisel RL (1988) The physiology of male sexual behaviour. In: Knobil E, Neill J (eds) The physiology of reproduction. Raven Press, New York, 1393–1485

    Google Scholar 

  • Satinoff E (1982) Are there similarities between thermoregulation and sexual behavior? In Pfaff D (ed) The physiological mechanisms of motivation. Springer, Berlin Heidelberg New York, pp 217–251

    Google Scholar 

  • Satinoff E, Ruttstein (1970) Behavioral thermoregulation in rats with anterior hypothalamic lesions. J comp physiol Psychol 71:77–82

    Google Scholar 

  • Slimp JC, Hart BL, Goy RW (1978) Heterosexual, autosexual and social behaviour of adult male rhesus monkeys with medial preoptic-anterior hypothalamic lesions. Brain Res 142:105–122

    Google Scholar 

  • Spyraki C, Fibiger HC, Phillips AG (1983) Attenuation of heroin reward in rats by disruption of the mesolimbic dopamine system. Psychopharmacologia 79:278–283

    Google Scholar 

  • Stavy M, Herbert J (1989) Differential effects of β-endorphin infused into the hypothalamic preoptic area at various phases of the male rat's sexual behaviour. Neuroscience 30:433–442

    Google Scholar 

  • Van der Kooy D (1985) Place conditioning: a simple and effective method for assessing the motivational properties of drugs. In: Bozarth MA (ed) Methods of assessing the reinforcing properties of abused drugs. Springer, Berlin Heidelberg New York, pp 229–240

    Google Scholar 

  • Wise RA (1989a) The brain and reward. In: Liebman JM, Cooper SJ (eds) Neuropharmacological basis of reward. Clarendon Press, Oxford, pp 377–424

    Google Scholar 

  • Wise RA (1989b) Opiate reward: sites and substrates. Neurosci Biobehav Rev 13:129–134

    Google Scholar 

  • Yim CY, Mogenson GJ (1982) Response of nucleus accumbens to amygdala stimulation and its modification by dopamine. Brain Res 239:401–415

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, University of Cambridge, Downing Street, CB2 3DY, Cambridge, UK

    A. M. Hughes, B. J. Everitt & J. Herbert

Authors
  1. A. M. Hughes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. J. Everitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Herbert
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hughes, A.M., Everitt, B.J. & Herbert, J. Comparative effects of preoptic area infusions of opioid peptides, lesions and castration on sexual behaviour in male rats: studies of instrumental behaviour, conditioned place preference and partner preference. Psychopharmacology 102, 243–256 (1990). https://doi.org/10.1007/BF02245929

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02245929

Key words

Search

Navigation