Differential disruption of conditioned ejaculatory preference in the male rat based on different sensory modalities by micro-infusions of naloxone to the medial preoptic area or ventral tegmental area
Male rats trained to associate a neutral odor or rodent jacket on a female with their post-ejaculatory reward state display a preference to ejaculate with females bearing the odor or jacket. This conditioned ejaculatory preference (CEP) can be shifted by systemic administration of the opioid antagonist naloxone (NAL) during training, such that NAL-trained males distribute their ejaculations to females without the cue, relative to saline (SAL)-trained males.
The present study examined two brain sites, the medial preoptic area (mPOA) or ventral tegmental area (VTA), where the opioid reward state might be induced.
Sexually naïve Long-Evans males were implanted with bilateral guide cannula aimed at either site before they underwent multi-ejaculatory conditioning trials at 4-day intervals with sexually receptive females that bore either an almond odor or rodent tethering jacket. Infusions of NAL (1 μl/side) or SAL (1 μl/side) were made prior to each conditioning trial. All males were infused with SAL prior to a final open-field choice test with two sexually receptive females, one scented and the other unscented, or one jacketed and the other unjacketed.
Males previously conditioned with SAL in either region showed significant CEP. In contrast, prior infusions of NAL to the mPOA shifted the preference towards the unfamiliar female, whereas prior infusions to the VTA abolished CEP for the odor. Subsequent detection of Fos protein induced by the cue showed that, relative to SAL-treated males, prior experience with NAL in the mPOA suppressed Fos in both the mPOA and VTA, whereas prior experience with NAL in to the VTA suppressed Fos in the VTA alone.
Opioid antagonism in the mPOA produces a state of non-reward whereas in the VTA, it produces a state in which the odor does not acquire incentive properties.
KeywordsConditioned ejaculatory preference Opioid mPOA VTA
This research was funded by a grant from the Canadian Institutes for Health Research (MOP-74563) to JGP, a graduate studentship from the Consejo Nacional de Ciencia y Tecnología de Chile to GRQ, and an infrastructure grant from Fonds de la Reserche en Santé du Québec to the Center for Studies in Behavioral Neurobiology at Concordia University.
Compliance with ethical standards
The authors declare that all animal procedures conformed to the guidelines of the Canadian Council for Animal Care. All procedures were approved by the Concordia University Animal Research Ethics Committee.
Conflict of interest
The authors declare they have no conflicts of interest.
- Arletti R, Calza L, Giardino L, Benelli A, Cavazzuti E, Bertolini A (1997) Sexual impotence is associated with a reduced production of oxytocin and with an increased production of opioid peptides in the paraventricular nucleus of male rats. Neurosci Lett 233:65–68PubMedCrossRefPubMedCentralGoogle Scholar
- Graham MD, Payne JW, Germé K, Pfaus JG (in press) Steroid hormones modulate dopamine receptor subtypes on glutamate and GABA neurons in the medial preoptic area of female rats that project to the ventromedial hypothalamus and ventral tegmental area: a triple-labelling study. Eur J NeurosciGoogle Scholar
- Institute for the Laboratory Animal Research (2011) Guide for the care and use of laboratory animals, 8th edn. National Academies Press, Washington (DC)Google Scholar
- Kallo I, Molnár CS, Szöke S, Fekete C, Hrabovszky E, Liposits Z (2015) Area-specific analysis of the distribution of hypothalamic neurons projecting to the rat ventral tegmental area, with special reference to the GABAergic and glutamatergic efferents. Front Neuroanat 9:112PubMedPubMedCentralCrossRefGoogle Scholar
- Kippin TE, Pfaus JG (2001) The development of olfactory conditioned ejaculatory preferences in the male rat I. Nature of the unconditioned stimulus. Behav Brain Res 73:457–469Google Scholar
- Lett BT, Grant VL, Koh MT (2001) Naloxone attenuates the conditioned place preference induced by wheel running in rats. Physiol Behav 72355–358.Google Scholar
- Lyilikci O, Balthazart J, Ball GF (2017) Medial preoptic regulation of the ventral tegmental area related to the control of sociosexual behaviors. eNeuro 3:1–12Google Scholar
- Quintana GR, González B, Borduas E, Lemay V, Yarur Y, Pfaus JG (2019b) Naloxone disrupts the development of a conditioned ejaculatory preference based on a somatosensory cue in male rats. Behav Neurosci 133(2):199–202Google Scholar