Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: comparison with novelty and locomotion.

Extracellular concentrations of dopamine (DA) and its metabolites dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) were examined concurrently, using in vivo microdialysis, in the nucleus accumbens and dorsal striatum of sexually active male rats during tests of locomotor activity, exposure to a novel chamber, exposure to sex odors, the presentation of a sexually receptive female, and copulation. DA increased significantly in the nucleus accumbens when the males were presented with a sexually receptive female behind a screen and increased further during copulation. Although DA also increased significantly in the dorsal striatum during copulation, the magnitude of the effect was significantly lower than that observed in the nucleus accumbens. In contrast, forced locomotion on a rotating drum, exposure to a novel chamber, and exposure to sex odors did not increase DA significantly in either region, although both DOPAC and HVA increased significantly in both regions during the locomotion test. These results indicate that novelty or locomotor activity alone cannot account for the increased extracellular DA concentrations observed in the nucleus accumbens of male rats during the presentation of a sexually receptive female behind a screen, nor can they account for the increased DA concentrations observed in both the nucleus accumbens and dorsal striatum of male rats during copulation. The preferential increase in DA transmission in the nucleus accumbens, compared with that in the striatum, suggests that anticipatory and consummatory aspects of sexual activity may belong to a class of naturally occurring events with reward values that are mediated by DA release in the nucleus accumbens. Much of the evidence linking central dopamine (DA) systems to the control of mammalian sexual behavior comes from pharmacological analyses in rats. Systemic administration of DA receptor agonists stimulates anticipatory and

[1]  T. Robbins,et al.  Interactions between the amygdala and ventral striatum in stimulus-reward associations: Studies using a second-order schedule of sexual reinforcement , 1989, Neuroscience.

[2]  J. B. Justice,et al.  Model studies for brain dialysis , 1983, Brain Research Bulletin.

[3]  G. Chiara,et al.  Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats , 1989, Neuroscience.

[4]  D. A. Edwards,et al.  Midbrain lesions, dopamine and male sexual behavior , 1986, Behavioural Brain Research.

[5]  H. Meltzer,et al.  Psychopharmacology : the third generation of progress , 1987 .

[6]  S. Cooper,et al.  The Neuropharmacological basis of reward , 1989 .

[7]  P. Willner,et al.  The Mesolimbic Dopamine System: From Motivation to Action An International Workshop Malta September 25–29, 1989 , 1989, Psychobiology.

[8]  A. Phillips,et al.  Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. , 1991, Behavioral neuroscience.

[9]  B. Everitt Sexual motivation: A neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats , 1990, Neuroscience & Biobehavioral Reviews.

[10]  A. Phillips,et al.  Influence of inherent directional biases on neurochemical consequences of conditioned circling. , 1989, Behavioral neuroscience.

[11]  R. Wise,et al.  A psychomotor stimulant theory of addiction. , 1987, Psychological review.

[12]  B. Yamamoto,et al.  Regional brain dopamine metabolism: a marker for the speed, direction, and posture of moving animals. , 1985, Science.

[13]  T. Robinson,et al.  Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with (+)-amphetamine: a microdialysis study in freely moving rats , 1988, Brain Research.

[14]  E. Hull,et al.  Regulation of Male Rat Copulatory Behavior by Preoptic Incertohypothalamic Dopamine Neurons' , 1987 .

[15]  H. Fibiger,et al.  Effects of Transient Forebrain Ischemia and Pargyline on Extracellular Concentrations of Dopamine, Serotonin, and Their Metabolites in the Rat Striatum as Determined by In Vivo Microdialysis , 1990, Journal of neurochemistry.

[16]  A. Phillips,et al.  Conditioned place preference as a measure of drug reward. , 1989 .

[17]  R. J. Barfield,et al.  Correlation of dopamine release in the nucleus accumbens with masculine sexual behavior in rats , 1990, Brain Research.

[18]  G. Di Chiara,et al.  Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[19]  T. Robinson,et al.  Enduring changes in brain and behavior produced by chronic amphetamine administration: A review and evaluation of animal models of amphetamine psychosis , 1986, Brain Research Reviews.

[20]  E. Hull,et al.  Dopaminergic control of male sex behavior in rats: Effects of an intracerebrally-infused agonist , 1986, Brain Research.

[21]  L. Pellegrino,et al.  stereotaxic atlas of the rat brain , 1967 .

[22]  F. D. Sheffield,et al.  Reward value of copulation without sex drive reduction. , 1951, Journal of comparative and physiological psychology.

[23]  U. Ungerstedt,et al.  Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. , 1970, Brain research.

[24]  R. Roth,et al.  Central dopaminergic neurons: effects of alterations in impulse flow on the accumulation of dihydroxyphenylacetic acid. , 1976, European journal of pharmacology.

[25]  B. Yamamoto,et al.  The trained circling rat: a model for inducing unilateral caudate dopamine metabolism , 1982, Nature.

[26]  J. Engel,et al.  Brain Reward Systems and Abuse , 1987 .

[27]  J. V. van Rossum,et al.  Effects of chemical stimulation of the mesolimbic dopamine system upon locomotor activity. , 1976, European journal of pharmacology.

[28]  S. Iversen,et al.  Selective 60HDA-induced destruction of mesolimbic dopamine neurons: Abolition of psychostimulant-induced locomotor activity in rats , 1976 .

[29]  E. Hull,et al.  Microinjection of the dopamine antagonist cis-flupenthixol into the MPOA impairs copulation, penile reflexes and sexual motivation in male rats , 1991, Brain Research.

[30]  E. Hull,et al.  Microinjection of Cis-flupenthixol, a Dopamine Antagonist, into the Medial Preoptic Area Impairs Sexual Behavior of Male Rats , 1987 .

[31]  F. S. Radhakishun,et al.  Scheduled eating increases dopamine release in the nucleus accumbens of food-deprived rats as assessed with on-line brain dialysis , 1988, Neuroscience Letters.

[32]  R. E. Whalen Effects of mounting without intromission and intromission without ejaculation on sexual behavior and maze learning. , 1961, Journal of comparative and physiological psychology.

[33]  G. Di Chiara,et al.  Dopamine release and metabolism in awake rats after systemic neuroleptics as studied by trans-striatal dialysis. , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  A. Louilot,et al.  Increased dopamine release in the nucleus accumbens of copulating male rats as evidenced by in vivo voltammetry , 1990, Neuroscience Letters.

[35]  B. Hoebel,et al.  Feeding and hypothalamic stimulation increase dopamine turnover in the accumbens , 1988, Physiology & Behavior.

[36]  J. Richards,et al.  In vivo dialysis measurements of dopamine and DOPAC in rats trained to turn on a circular treadmill , 1990, Pharmacology Biochemistry and Behavior.

[37]  A. Phillips,et al.  Bilateral augmentation of dopaminergic and serotonergic activity in the striatum and nucleus accumbens induced by conditioned circling , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Ian Q. Whishaw,et al.  Normalization of extracellular dopamine in striatum following recovery from a partial unilateral 6-OHDA lesion of the substantia nigra: a microdialysis study in freely moving rats , 1988, Brain Research.

[39]  A. Monaco,et al.  Self-injection of amphetamine directly into the brain , 2004, Psychopharmacology.

[40]  J. Falk Physiology and Behavior. , 1973 .

[41]  G. Rebec,et al.  Critical issues in assessing the behavioral effects of amphetamine , 1984, Neuroscience & Biobehavioral Reviews.

[42]  T. Robbins,et al.  Limbic-striatal interactions in reward-related processes , 1989, Neuroscience & Biobehavioral Reviews.

[43]  H. Fibiger,et al.  Sexual behavior enhances central dopamine transmission in the male rat , 1990, Brain Research.

[44]  R. Miller,et al.  Naloxone inhibits mating and conditioned place preference for an estrous female in male rats soon after castration , 1987, Pharmacology Biochemistry and Behavior.

[45]  A. Phillips,et al.  A correlational and factor analysis of anticipatory and consummatory measures of sexual behavior in the male rat , 1990, Psychoneuroendocrinology.

[46]  C. A. Marsden,et al.  Measurement of neurotransmitter release in vivo , 1984 .

[47]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[48]  D. S. Zahm,et al.  Specificity in the projection patterns of accumbal core and shell in the rat , 1991, Neuroscience.