Colocalization of mating-induced Fos and D2-like dopamine receptors in the medial preoptic area: Influence of sexual experience

Frontiers in Behavioral Neuroscience

Volumn 10, Issue APRIL, 2016, Pages

  Nutsch, Victoria L ^a   Will, Ryan G ^a   Robison, Christopher L ^a   Martz, Julia R ^a   Tobiansky, Daniel J ^a   Dominguez, Juan M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Copulation; D2 dopamine receptors; Dopamine; Fos; Preoptic area; Sexual experience

Indexed keywords

DOPAMINE 2 RECEPTOR; PROTEIN FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; COPULATION; EJACULATION; EXPERIENCE; IMMUNOHISTOCHEMISTRY; MALE; MEDIAL PREOPTIC AREA; NONHUMAN; PROTEIN LOCALIZATION; RAT; RECEPTOR DENSITY; SEXUAL BEHAVIOR;

EID: 84966728783     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2016.00075     Document Type: Article

References (61)

1. Balthazart, J., Castagna, C., and Ball, G. F. (1997). Differential effects of D1 and D2 dopamine-receptor agonists and antagonists on appetitive and consummatory aspects of male sexual behavior in Japanese quail. Physiol. Behav. 62, 571-580. doi: 10.1016/s0031-9384(97)00163-7
2. Baum, M. J., and Everitt, B. J. (1992). Increased expression of c-fos in the medial preoptic area after mating in male rats: role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience 50, 627-646. doi: 10.1016/0306-4522(92)90452-8
3. Bitran, D., Hull, E. M., Holmes, G. M., and Lookingland, K. J. (1988). Regulation of male rat copulatory behavior by preoptic incertohypothalamic dopamine neurons. Brain Res. Bull. 20, 323-331. doi: 10.1016/0361-9230(88)90062-7
4. Björklund, A., Lindvall, O., and Nobin, A. (1975). Evidence of an incerto-hypothalamic dopamine neurone system in the rat. Brain Res. 89, 29-42. doi: 10.1016/0006-8993(75)90131-6
5. Boundy, V. A., Luedtke, R. R., Artymyshyn, R. P., Filtz, T. M., and Molinoff, P. B. (1993). Development of polyclonal anti-D2 dopamine receptor antibodies using sequence-specific peptides. Mol. Pharmacol. 43, 666-676. doi: 10.1111/j.1471-4159.1993.tb03504.x
6. Bressler, S. C., and Baum, M. J. (1996). Sex comparison of neuronal Fos immunoreactivity in the rat vomeronasal projection circuit after chemosensory stimulation. Neuroscience 71, 1063-1072. doi: 10.1016/0306-4522(95)00493-9
7. Carney, J. M., Tolliver, B., Carney, J. P., and Kindy, M. S. (1991). Selective effects of behaviorally active doses of methamphetamine on mRNA expression in the gerbil brain. Neuropharmacology 30, 1011-1019. doi: 10.1016/0028-3908(91)90114-q
8. Da Prada, M., Carruba, M., Saner, A., O’Brien, A., and Pletscher, A. (1973). The action L-DOPA on sexual behaviour of male rats. Brain Res. 55, 383-389. doi: 10.1016/0006-8993(73)90303-x
9. Dominguez, J. M. (2009). A role for preoptic glutamate in the regulation of male reproductive behavior. Neuroscientist 15, 11-19. doi: 10.1177/1073858408322679
10. Dominguez, J. M., Gil, M., and Hull, E. M. (2006). Preoptic glutamate facilitates male sexual behavior. J. Neurosci. 26, 1699-1703. doi: 10.1523/JNEUROSCI.4176-05.2006
11. Dominguez, J. M., and Hull, E. M. (2005). Dopamine, the medial preoptic area and male sexual behavior. Physiol. Behav. 86, 356-368. doi: 10.1016/j.physbeh.2005.08.006
12. Farooqui, S. M., Prasad, C., and Ali, M. (1992). Production and characterization of a monoclonal antibody to dopamine D2 receptor: comparison with a polyclonal antibody to a different epitope. Biochem. Biophys. Res. Commun. 184, 661-667. doi: 10.1016/0006-291x(92)90640-7
13. Ferrari, F., Ottani, A., and Giuliani, D. (2002). Influence of sildenafil on central dopamine-mediated behaviour in male rats. Life Sci. 70, 1501-1508. doi: 10.1016/s0024-3205(01)01515-6
14. Gerfen, C. R., Keefe, K. A., and Gauda, E. B. (1995). D1 and D2 dopamine receptor function in the striatum: coactivation of D1- and D2-dopamine receptors on separate populations of neurons results in potentiated immediate early gene response in D1-containing neurons. J. Neurosci. 15, 8167-8176.
15. Gil, M., Bhatt, R., Picotte, K. B., and Hull, E. M. (2011). Oxytocin in the medial preoptic area facilitates male sexual behavior in the rat. Horm. Behav. 59, 435-443. doi: 10.1016/j.yhbeh.2010.12.012
16. Gingrich, J. A., and Caron, M. G. (1993). Recent advances in the molecular biology of dopamine receptors. Annu. Rev. Neurosci. 16, 299-321. doi: 10.1146/annurev.neuro.16.1.299
17. Giuliano, F., Bernabé, J., Brown, K., Droupy, S., Benoit, G., and Rampin, O. (1997). Erectile response to hypothalamic stimulation in rats: Role of peripheral nerves. Am. J. Physiol. 273, R1990-R1997.
18. Graybiel, A. M., Moratalla, R., and Robertson, H. A. (1990). Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc. Natl. Acad. Sci. U S A 87, 6912-6916. doi: 10.1073/pnas.87.17.6912
19. Hull, E. M., Bitran, D., Pehek, E. A., Warner, R. K., and Band, L. C. (1986). Dopaminergic control of male sex behavior in rats: effects of an intracerebrally infused agonist. Brain Res. 370, 73-81. doi: 10.1016/0006-8993(86)91106-6
20. Hull, E. M., and Dominguez, J. M. (2006). Getting his act together: roles of glutamate, nitric oxide and dopamine in the medial preoptic area. Brain Res. 1126, 66-75. doi: 10.1016/j.brainres.2006.08.031
21. Hull, E. M., and Dominguez, J. M. (2015). “Male sexual behavior,” in Knobil and Neill’s Physiology of Reproduction, 4th Edn, eds T. M. Plant and A. J. Zeleznik (New York, NY: Elsevier), 2211-2285.
22. Hull, E. M., Eaton, R. C., Markowski, V. P., Moses, J., Lumley, L. A., and Loucks, J. A. (1992). Opposite influence of medial preoptic Dl and D2 receptors on genital reflexes: implications for copulation. Life Sci. 51, 1705-1713. doi: 10.1016/0024-3205(92)90299-5
23. Hull, E. M., Lumley, L. A., Matuszewich, L., Dominguez, J., Moses, J., and Lorrain, D. S. (1994). The roles of nitric oxide in sexual function of male rats. Neuropharmacology 33, 1499-1504. doi: 10.1016/0028-3908(94)90054-x
24. Hull, E. M., Warner, R. K., Bazzett, T. J., Eaton, R. C., Thompson, J. T., and Scaletta, L. L. (1989). D2/D1 ratio in the medial preoptic area affects copulation of male rats. J. Pharmacol. Exp. Ther. 251, 422-427.
25. Keefe, K. A., and Gerfen, C. R. (1995). D1-D2 dopamine receptor synergy in striatum: effects of intrastriatal infusions of dopamine agonists and antagonists on immediate early gene expression. Neuroscience 66, 903-913. doi: 7651617
26. Kleitz-Nelson, H. K., Dominguez, J. M., and Ball, G. F. (2010a). Dopamine release in the medial preoptic area is related to hormonal action and sexual motivation. Behav. Neurosci. 124, 773-779. doi: 10.1037/a0021490
27. Kleitz-Nelson, H. K., Dominguez, J. M., Cornil, C. A., and Ball, G. F. (2010b). Is sexual motivational state linked to dopamine release in the medial preoptic area? Behav. Neurosci. 124, 300-304. doi: 10.1037/a0018767
28. Lidow, M. S., Goldman-Rakic, P. S., Rakic, P., and Innis, R. B. (1989). Dopamine D2 receptors in the cerebral cortex: distribution and pharmacological characterization with [3H]raclopride. Proc. Natl. Acad. Sci. U S A 86, 6412-6416. doi: 10.1073/pnas.86.16.6412
29. Malsbury, C. W. (1971). Facilitation of male rat copulatory behavior by electrical stimulation of the medial preoptic area. Physiol. Behav. 7, 797-805. doi: 10.1016/0031-9384(71)90042-4
30. Markowski, V. P., Eaton, R. C., Lumley, L. A., Moses, J., and Hull, E. M. (1994). A D1 agonist in the MPOA area facilitates copulation of male rats. Pharmacol. Biochem. Behav. 47, 483-486. doi: 10.1016/0091-3057(94)90147-3
31. Marson, L., and McKenna, K. E. (1994). Serotonergic neurotoxic lesions facilitate male sexual reflexes. Pharmacol. Biochem. Behav. 47, 883-888. doi: 10.1016/0091-3057(94)90292-5
32. McHenry, J. A., Bell, G. A., Parrish, B. P., and Hull, E. M. (2012). Dopamine D1 receptors and phosphorylation of dopamine- and cyclic AMP-regulated phosphoprotein-32 in the medial preoptic area are involved in experience-induced enhancement of male sexual behavior in rats. Behav. Neurosci. 126, 523-529. doi: 10.1037/a0028707
33. Meador-Woodruff, J. H., Mansour, A., Bunzow, J. R., Van Tol, H. H., Watson, S. J. Jr., Civelli, O. (1989). Distribution of D2 dopamine receptor mRNA in rat brain. Proc. Natl. Acad. Sci. U S A 86, 7625-7628. doi: 10.1073/pnas.86.19.7625
34. Mendelson, S. D., and Pfaus, J. G. (1989). Level searching: a new assay of sexual motivation in the male rat. Physiol Behav 45, 337-341. doi: 10.1016/0031-9384(89)90136-4
35. Miller, S. M., and Lonstein, J. S. (2009). Dopaminergic projections to the medial preoptic area of postpartum rats. Neuroscience 159, 1384-1396. doi: 10.1016/j.neuroscience.2009.01.060
36. Moore, K. E., and Lookingland, K. J. (1995). “Dopaminergic neuronal systems in the hypothalamus,” in Psychopharmacology: The Fourth Generation of Progress, eds F. E. Bloom and D. J. Kupfer (New York, NY: Raven Press), 245-246.
37. Moreira, I. S., Shi, L., Freyberg, Z., Ericksen, S. S., Weinstein, H., and Javitch, J. A. (2010). “Structural basis of dopamine receptor activation,” in The Dopamine Receptors, 2nd Edn, ed. K. A. Neve (New York, NY: Humana Press), 47-74.
38. Nutsch, V. L., Will, R. G., Hattori, T., Tobiansky, D. J., and Dominguez, J. M. (2014). Sexual experience influences mating-induced activity in nitric oxide synthase-containing neurons in the medial preoptic area. Neurosci. Lett. 579, 92-96. doi: 10.1016/j.neulet.2014.07.021
39. Oomura, Y., Aou, S., Koyama, Y., and Yoshimatsu, H. (1988). Central control of sexual behavior. Brain Res. Bull. 20, 863-870. doi: 10.1016/0361-9230(88)90103-7
40. Paglietti, E., Quarantotti, B. P., Mereu, G., and Gessa, G. L. (1978). Apomorphine and L-DOPA lower ejaculation threshold in the male rat. Physiol. Behav. 20, 559-562. doi: 10.1016/0031-9384(78)90247-0
41. Pehek, E. A., Thompson, J. T., Eaton, R. C., Bazzett, T. J., and Hull, E. M. (1988a). Apomorphine and haloperidol, but not domperidone, affect penile reflexes in rats. Pharmacol. Biochem. Behav. 31, 201-208. doi: 10.1016/0091-3057(88)90334-6
42. Pehek, E. A., Warner, R. K., Bazzett, T. J., Bitran, D., Band, L. C., and Eaton, R. C., et al. (1988b). Microinjection of cis-flupenthixol, a dopamine antagonist, into the medial preoptic area impairs sexual behavior of male rats. Brain Res. 443, 70-76. doi: 10.1016/0006-8993(88)91599-5
43. Pehek, E. A., Thompson, J. T., and Hull, E. M. (1989). The effects of intracranial administration of the dopamine agonist apomorphine on penile reflexes and seminal emission in the rat. Brain Res. 500, 325-332. doi: 10.1016/0006-8993(89)90328-4
44. Pfaus, J. G., and Heeb, M. M. (1997). Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res. Bull. 44, 397-407. doi: 10.1016/s0361-9230(97)00219-0
45. Pfaus, J. G., and Phillips, A. G. (1989). Differential effects of dopamine receptor antagonists on the sexual behavior of male rats. Psychopharmacology (Berl.) 98, 363-368. doi: 10.1007/bf00451688
46. Pfaus, J. G., and Phillips, A. G. (1991). Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behav. Neurosci. 105, 727-743. doi: 10.1037/0735-7044.105.5.727
47. Rampin, O., Jérôme, N., and Suaudeau, C. (2003). Proerectile effects of apomorphine in mice. Life Sci. 72, 2329-2336. doi: 10.1016/s0024-3205(03)00122-x
48. Robertson, G. S., Pfaus, J. G., Atkinson, L. J., Matsumura, H., Phillips, A. G., and Fibiger, H. C. (1991). Sexual behavior increases c-fos expression in the forebrain of the male rat. Brain Res. 564, 352-357. doi: 10.1016/0006-8993(91)91477-i
49. Rodríguez-Manzo, G., Pellicer, F., Larsson, K., and Fernández-Guasti, A. (2000). Stimulation of the medial preoptic area facilitates sexual behavior but does not reverse sexual satiation. Behav. Neurosci. 114, 553-560. doi: 10.1037/0735-7044.114.3.553
50. Sakata, M., Farooqui, S. M., and Prasad, C. (1992). Post-transcriptional regulation of loss of rat striatal D2 dopamine receptor during aging. Brain Res. 575, 309-314. doi: 10.1016/0006-8993(92)90095-q
51. Shimura, T., Yamamoto, T., and Shimokochi, M. (1994). The medial preoptic area is involved in both sexual arousal and performance in male rats: re-evaluation of neuron activity in freely moving animals. Brain Res. 640, 215-222. doi: 10.1016/0006-8993(94)91875-9
52. Sibley, D. R., and Monsma, F. J. Jr. (1992). Molecular biology of dopamine receptors. Trends Pharmacol. Sci. 13, 61-69. doi: 10.1016/0165-6147(92)90025-2
53. Simerly, R. B., and Swanson, L. W. (1986). The organization of neural inputs to the medial preoptic nucleus of the rat. J. Comp. Neurol. 246, 312-342. doi: 10.1002/cne.902460304
54. Simerly, R. B., and Swanson, L. W. (1988). Projections of the medial preoptic nucleus: a Phaseolis vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J. Comp. Neurol. 270, 209-242. doi: 10.1002/cne.902700205
55. Swaney, W. T., Dubose, B. N., Curley, J. P., and Champagne, F. A. (2012). Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice. Horm. Behav. 61, 472-478. doi: 10.1016/j.yhbeh.2012.01.001
56. Swanson, L. W. (2004). Brain Maps: Structure of the Rat Brain. San Diego, CA: Academic Press.
57. Tobiansky, D. J., Hattori, T., Scott, J. M., Nutsch, V. L., Roma, P. G., and Dominguez, J. M. (2012). Mating-relevant olfactory stimuli activate the rat brain in an age-dependent manner. Neuroreport 23, 1077-1083. doi: 10.1097/wnr.0b013e32835b6ec1
58. Veening, J. G., and Coolen, L. M. (1998). Neural activation following sexual behavior in the male and female rat brain. Behav. Brain Res. 92, 181-193. doi: 10.1016/s0166-4328(97)00190-3
59. Will, R. G., Nutsch, V. L., Turner, J. M., Hattori, T., Tobiansky, D. J., and Dominguez, J. M. (2015). Astrocytes in the medial preoptic area modulate ejaculation latency in an experience-dependent fashion. Behav. Neurosci. 129, 68-73. doi: 10.1037/bne0000026
60. Wirtshafter, D., and Krebs, J. C. (1997). Interactive effects of stimulation of D1 and D2 dopamine receptors on Fos expression in the lateral habenula. Brain Res. 750, 245-250. doi: 10.1016/s0006-8993(96)01353-4
61. Young, S. T., Porrino, L. J., and Iadarola, M. J. (1991). Cocaine induces striatal c-fos-immunoreactive proteins via dopaminergic D1 receptors. Proc. Natl. Acad. Sci. U S A 88, 1291-1295. doi: 10.1073/pnas.88.4.1291