Adolescent brain maturation is necessary for adult-typical mesocorticolimbic responses to a rewarding social cue

Developmental Neurobiology

Volumn 73, Issue 11, 2013, Pages 856-869

  Bell, Margaret R ^a   Meerts, Sarah H ^b   Sisk, Cheryl L ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b CARLETON COLLEGE   (United States)

Author keywords

Dopamine; Fos; Pheromone; Puberty; Testosterone

Indexed keywords

DOPAMINE; ESTRADIOL BENZOATE; MINERAL OIL; PROGESTERONE; PROTEIN FOS; SEX PHEROMONE; TESTOSTERONE; TYROSINE 3 MONOOXYGENASE;

ADOLESCENT DEVELOPMENT; ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN MATURATION; BRAIN REGION; CELL DENSITY; CONTROLLED STUDY; FEMALE; GONADECTOMY; HAMSTER; HISTOLOGY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; JUVENILE ANIMAL; LIMBIC CORTEX; MALE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RECEPTOR BINDING; SEXUAL BEHAVIOR; SOCIAL INTERACTION; TESTOSTERONE BLOOD LEVEL; VAGINAL SECRETION;

DOPAMINE; FOS; PHEROMONE; PUBERTY; TESTOSTERONE;

AGING; ANIMALS; BRAIN; CRICETINAE; CUES; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MESOCRICETUS; REWARD; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

EID: 84885429766     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22106     Document Type: Article

References (67)

1. Alderson LM, Baum MJ. 1981. Differential effects of gonadal steroids on dopamine metabolism in mesolimbic and nigro-striatal pathways of male rat brain. Brain Res 218:189-206.
2. Andersen SL, Rutstein M, Benzo JM, Hostetter JC, Teicher MH. 1997. Sex differences in dopamine receptor overproduction and elimination. Neuroreport 8:1495-1498.
3. Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH. 2000. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167-169.
4. Aubele T, Kritzer MF. 2011. Gonadectomy and hormone replacement affects in vivo basal extracellular dopamine levels in the prefrontal cortex but not motor cortex of adult male rats. Cereb Cortex 21:222-232.
5. Aubele T, Kritzer MF. 2012. Androgen influence on prefrontal dopamine systems in adult male rats: Localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level. Cereb Cortex 22:1799-1812.
6. Aumann TD, Egan K, Lim J, Boon WC, Bye CR, Chua HK, Baban N, Parish CL, Bobrovskaya L, Dickson P, Horne MK. 2011. Neuronal activity regulates expression of tyrosine hydroxylase in adult mouse substantia nigra pars compacta neurons. J Neurochem 116:646-658.
7. Baum MJ, Melamed E, Globus M. 1986. Dissociation of the effects of castration and testosterone replacement on sexual behavior and neural metabolism of dopamine in the male rat. Brain Res Bull 16:145-148.
8. Becker JB, Rudick CN, Jenkins WJ. 2001. The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. J Neurosci 21:3236-3241.
9. Bell MR, De Lorme KC, Figueira RJ, Kashy DA, Sisk CL. 2013. Adolescent gain in positive valence of a socially relevant stimulus: Engagement of the mesocorticolimbic reward circuitry. Eur J Neurosci 37:457-468.
10. Bell MR, Meerts SH, Sisk CL. 2010. Male Syrian hamsters demonstrate a conditioned place preference for sexual behavior and female chemosensory stimuli. Horm Behav 58:410-414.
11. Bell MR, Sisk CL. 2013. Dopamine mediates testosterone-induced social reward in male Syrian hamsters. Endocrinology 154:1225-1234.
12. Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Hervé D, Valjent E, Girault J-A. 2008. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28:5671-5685.
13. Brenhouse HC, Sonntag KC, Andersen SL. 2008. Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: Relationship to enhanced motivational salience of drug cues in adolescence. J Neurosci 28:2375-2382.
14. Coolen LM, Wood RI. 1998. Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: Simultaneous anterograde and retrograde tract tracing. J Comp Neurol 399:189-209.
15. Creese I, Sibley DR, Leff S. 1983. Classification of dopamine receptors. Adv Biochem Psychopharmacol 37:255-266.
16. Cunningham MG, Bhattacharyya S, Benes FM. 2002. Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. J Comp Neurol 453:116-130.
17. David HN, Ansseau M, Abraini JH. 2005. Dopamine-glutamate reciprocal modulation of release and motor responses in the rat caudate-putamen and nucleus accumbens of "intact" animals. Brain Res Rev 50:336-360.
18. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP. 2010. Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn 72:114-123.
19. Engel J, Ahlenius S, Almgren O, Carlsson A, Larsson K, Södersten P. 1979. Effects of gonadectomy and hormone replacement on brain monoamine synthesis in male rats. Pharmacol Biochem Behav 10:149-154.
20. Fiber JM, Adames P, Swann JM. 1993. Pheromones induce c-fos in limbic areas regulating male hamster mating behavior. Neuroreport 4:871-874.
21. Fiber JM, Swann JM. 1996. Testosterone differentially influences sex-specific pheromone-stimulated Fos expression in limbic regions of Syrian hamsters. Horm Behav 30:455-473.
22. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490:270-294.
23. Giorgi O, De Montis G, Porceddu ML, Mele S, Calderini G, Toffano G, Biggio G. 1987. Developmental and age-related changes in D1-dopamine receptors and dopamine content in the rat striatum. Brain Res 432:283-290.
24. Grace AA. 1991. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia. Neuroscience 41:1-24.
25. Hughes P, Dragunow M. 1995. Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol Rev 47:133-178.
26. Hull EM, Du J, Lorrain DS, Matuszewich L. 1995. Extracellular dopamine in the medial preoptic area: Implications for sexual motivation and hormonal control of copulation. J Neurosci 15:7465-7471.
27. Hunt GE, McGregor IS. 1997. Rewarding brain stimulation induces only sparse Fos-like immunoreactivity in dopaminergic neurons. Neuroscience 83:501-515.
28. Ikemoto S. 2007. Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27-78.
29. Johnson ML, Day AE, Ho CC, Walker QD, Francis R, Kuhn CM. 2010. Androgen decreases dopamine neurone survival in rat midbrain. J Neuroendocrinol 22:238-247.
30. Johnston RE, Coplin B. 1979. Development of responses to vaginal secretion and other substances in golden hamsters. Behav Neural Biol 25:473-489.
31. Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings HB. 1988. Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol 269:58-72.
32. Keefe KA, Gerfen CR. 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.
33. Kevetter GA, Winans SS. 1981. Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the "vomeronasal amygdala". J Comp Neurol 197:81-98.
34. Kollack-Walker S, Newman SW. 1997. Mating-induced expression of c-fos in the male Syrian hamster brain: Role of experience, pheromones, and ejaculations. J Neurobiol 32:481-501.
35. Kollack-Walker S, Watson SJ, Akil H. 1997. Social stress in hamsters: Defeat activates specific neurocircuits within the brain. J Neurosci 17:8842-55.
36. Kritzer MF, Brewer A, Montalmant F, Davenport M, Robinson JK. 2007. Effects of gonadectomy on performance in operant tasks measuring prefrontal cortical function in adult male rats. Horm Behav 51:183-194.
37. Luo Z, Volkow ND, Heintz N, Pan Y, Du C. 2011. Acute cocaine induces fast activation of D1 receptor and progressive deactivation of D2 receptor striatal neurons: In vivo optical microprobe [Ca2+]i imaging. J Neurosci 31:13180-13190.
38. Mathews IZ, Waters P, McCormick CM. 2009. Changes in hyporesponsiveness to acute amphetamine and age differences in tyrosine hydroxylase immunoreactivity in the brain over adolescence in male and female rats. Dev Psychobiol 51:417-428.
39. McArthur S, Murray HE, Dhankot A, Dexter DT, Gillies GE. 2007. Striatal susceptibility to a dopaminergic neurotoxin is independent of sex hormone effects on cell survival and DAT expression but is exacerbated by central aromatase inhibition. J Neurochem 100:678-692.
40. Meek LR, Romeo RD, Novak CM, Sisk CL. 1997. Actions of testosterone in prepubertal and postpubertal male hamsters: Dissociation of effects on reproductive behavior and brain androgen receptor immunoreactivity. Horm Behav 31:75-88.
41. Meisel RL, Joppa MA, Rowe RK. 1996. Dopamine receptor antagonists attenuate conditioned place preference following sexual behavior in female Syrian hamsters. Eur J Pharmacol 309:21-24.
42. Miller LL, Whitsett JM, Vandenberg, JG, Colby DR. 1977. Physical and Behavioral Aspects of Sexual Maturation in Male Golden Hamsters. J Comp Phy Psych 91:245-259.
43. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG. 1998. Dopamine receptors: From structure to function. Physiol Rev 78:189-225.
44. Mitchell JB, Stewart J. 1989. Effects of castration, steroid replacement, and sexual experience on mesolimbic dopamine and sexual behaviors in the male rat. Brain Res 491:116-127.
45. Morin LP, Woods R. 2001. A Stereotaxic Atlas of the Golden Hamster Brain. London, UK: Academic Press.
46. Oades RD, Halliday GM. 1987. Ventral tegmental (A10) system: Neurobiology. 1. Anatomy and connectivity. Brain Res 434:117-165.
47. Olson VG, Zabetian CP, Bolanos CA, Edwards S, Barrot M, Eisch AJ, Hughes T, et al. 2005. Regulation of drug reward by cAMP response element-binding protein: Evidence for two functionally distinct subregions of the ventral tegmental area. J Neurosci 25:5553-5562.
48. Phillipson OT. 1979. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: A horseradish peroxidase study in the rat. J Comp Neurol 187:117-143.
49. Putnam SK, Du J, Sato S, Hull EM. 2001. Testosterone restoration of copulatory behavior correlates with medial preoptic dopamine release in castrated male rats. Horm Behav 39:216-224.
50. Putnam SK, Sato S, Hull EM. 2003. Effects of testosterone metabolites on copulation and medial preoptic dopamine release in castrated male rats. Horm Behav 44:419-426.
51. Richfield EK, Penney JB, Young AB. 1989. Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience 30:767-777.
52. Romeo RD, Parfitt DB, Richardson HN, Sisk CL. 1998. Pheromones elicit equivalent levels of Fos immunoreactivity in prepubertal and adult male Syrian hamsters. Horm Behav 34:48-55.
53. Schulz KM, Sisk CL. 2006. Pubertal hormones, the adolescent brain, and the maturation of social behaviors: Lessons from the Syrian hamster. Mol Cell Endocrinol 254-255:120-126.
54. Schulz KM, Zehr JL, Salas-Ramirez KY, Sisk CL. 2009. Testosterone programs adult social behavior before and during, but not after, adolescence. Endocrinology 150:3690-3698.
55. Sesack SR, Grace AA. 2010. Cortico-Basal Ganglia reward network: Microcircuitry. Neuropsychopharmacology 35:27-47.
56. Sheng M, Greenberg ME. 1990. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477-485.
57. Spear LP. 2000. The adolescent brain and age-related behavioral manifestations. Neurobehavioral changes in adolescence. Curr Dir Psycholog Sci 24:417-463.
58. Stork O, Hashimoto T, Obata K. 1994. Haloperidol activates tyrosine hydroxylase gene-expression in the rat substantia nigra, pars reticulata. Brain Res 633:213-222.
59. Swanson LW. 1982. The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321-353.
60. Tarazi FI, Baldessarini RJ. 2000. Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 18:29-37.
61. Thompson RH, Swanson LW. 2010. Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc Natl Acad Sci USA 107:15235-15239.
62. Vandenbergh JG. 1973. Effects of gonadal hormones on the flank gland of the golden hamster. Horm Res 4:28-33.
63. Vincent SR. 1988. Distributions of tyrosine hydroxylase-, dopamine-beta-hydroxylase-, and phenylethanolamine-N-methyltransferase-immunoreactive neurons in the brain of the hamster (Mesocricetus auratus). J Comp Neurol 268:584-599.
64. Wahlstrom D, White T, Luciana M. 2010. Neurobehavioral evidence for changes in dopamine system activity during adolescence. Neurosci Biobehav Rev 34:631-648.
65. Wirtshafter D, Asin KE. 1994. Interactive effects of stimulation of D1 and D2 dopamine receptors on fos-like immunoreactivity in the normosensitive rat striatum. Brain Res Bull 35:85-91.
66. Wood RI. 1997. Thinking about networks in the control of male hamster sexual behavior. Horm Behav 32:40-45.
67. Wood RI, Newman SW. 1995. Integration of chemosensory and hormonal cues is essential for mating in the male Syrian hamster. J Neurosci 15:7261-7269.