Cited by 23Neuroendocrine regulation and behaviorSexual Differentiation and DisordersOlfactory and Sensory Function Studies

Androgenic and oestrogenic influences on tyrosine hydroxylase-immunoreactive cells of the prairie vole medial amygdala and bed nucleus of the stria terminalis

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Cavanaugh, B. L., Lonstein, J. S.·2010·Journal of Neuroendocrinology

Abstract

The posterodorsal medial amygdala (MeApd) and principal nucleus of the bed nucleus of the stria terminalis (pBST) are densely interconnected sites integrating steroid hormone and olfactory information necessary for sociosexual behaviours in many rodents. Our laboratory recently reported sexually dimorphic populations of cells containing tyrosine hydroxylase (TH) located in the MeApd and pBST of prairie voles (Microtus ochrogaster), with males having many more TH‐immunoreactive (‐ir) cells in these sites than do females. Gonadal hormones circulating during adulthood were showm to regulate this sex difference because it was eliminated by castrating adult males or implanting females with testosterone‐filled capsules. In the present study, we demonstrate that many (25–65%) TH‐ir cells in the MeApd and pBST of adult virgin male and female prairie voles also contain immunoreactivity for either the androgen receptor or oestrogen receptor α. Subcutaneous implants of oestradiol benzoate mimicked the effects of testosterone and maintained high numbers of TH‐ir cells in these sites in castrated males. However, implants of dihydrotestosterone (DHT) did not, and these males had low numbers of TH‐ir cells similar to castrated males given empty capsules. A similar effect was found in females, where testosterone or oestradiol benzoate greatly increased the number of TH‐ir cells in these sites compared to intact or ovariectomised controls, but DHT did not. DHT implants did, however, maintain high seminal vesicle weights in males. Thus, many of the TH‐ir cells in the prairie vole MeApd and pBST are potentially sensitive to androgens and oestrogens, although maintaining immunocytochemically detectable levels of TH in these cells may depend more on an oestrogen‐mediated mechanism in both sexes. These data have implications for understanding how gonadal hormone release across the reproductive cycle modulates these species‐specific groups of catecholaminergic cells and socially monogamous behaviours in prairie voles.

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Crossref · 10.1111/j.1365-2826.2010.01958.x

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  • Because AVP/OT and the dopaminergic pathways they feed into are heavily influenced by sex steroids across the lifespan, their sexually dimorphic ontogeny and function may be particularly vulnerable to endocrine disruption.

    “Because AVP/OT and the dopaminergic pathways they feed into are heavily influenced by sex steroids across the lifespan (50–59), it is highly plausible that their sexually dimorphic ontogeny and function may be particularly vulnerable to endocrine disruption.”

    From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [55]

    The Abstract reports that sex steroids regulate sexually dimorphic tyrosine hydroxylase-immunoreactive cells in adult prairie voles. The Discussion also describes hormone-mediated plasticity in adult cells synthesizing vasopressin. These passages do not establish steroid effects on oxytocin or effects across the lifespan; the endocrine-disruption inference is the citing authors’ own conclusion, not a finding attributed to this source. (LLM, conf=0.86)

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Research works printed but not linked: 53

  1. [1]Newman SW The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network Ann N Y Acad Sci 1999 877 242 57 10415653
  2. [2]Kang N Baum MJ Cherry JA A direct main olfactory bulb projection to the ‘vomeronasal’ amygdala in female mice selectively responds to volatile pheromones from males Eur J Neurosci 2009 29 624 34 19187265 PMC2669936
  3. [4]Pro-Sistiaga P Mohedano-Moriano A Ubeda-Bañon I de la Rosa-Prieto C Saiz-Sanchez D Martinez-Marcos A Projections of olfactory bulbs to the olfactory and vomeronasal cortices Neuroreport 2008 19 1541 4 18797313
  4. [5]Scalia F Winans SS The differential projections of the olfactory bulb and accessory olfactory bulb in mammals J Comp Neurol 1975 161 31 55 1133226
  5. [6]Winans SS Scalia F Amygdaloid nucleus: new afferent input from the vomeronasal organ Science 1970 170 330 2 5460037
  6. [7]de Jonge FH Oldenburger WP Louwerse AL Van de Poll NE Changes in male copulatory behavior after sexual exciting stimuli: effects of medial amygdala lesions Physiol Behav 1992 52 327 32 1523261
  7. [8]Kondo Y Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats Physiol Behav 1992 51 939 43 1615054
  8. [9]Kondo Y Sachs BD Sakuma Y Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females Behav Brain Res 1998 91 215 22 9578453
  9. [10]McGregor A Herbert J Differential effects of excitotoxic basolateral and corticomedial lesions of the amygdala on the behavioural and endocrine responses to either sexual or aggression-promoting stimuli in the male rat Brain Res 1992 574 9 20 1386276
  10. [11]Kondo Y Sakuma Y The medial amygdala controls the coital access of female rats: a possible involvement of emotional responsiveness Jpn J Physiol 2005 55 345 53 16409669
  11. [12]Fleming AS Vaccarino F Luebke C Amygdaloid inhibition of maternal behavior in the nulliparous female rat Physiol Behav 1980 25 731 43 7443835
  12. [13]Petrulis A Neural mechanisms of individual and sexual recognition in Syrian hamsters (Mesocricetus auratus) Behav Brain Res 2009 200 260 7 19014975 PMC2668739
  13. [14]Canteras NS Simerly RB Swanson LW Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat J Comp Neurol 1995 360 213 45 8522644
  14. [16]von Campenhausen H Mori K Convergence of segregated pheromonal pathways from the accessory olfactory bulb to the cortex in the mouse Eur J Neurosci 2000 12 33 46 10651858
  15. [17]Alheid GF Extended amygdala and basal forebrain Ann N Y Acad Sci 2003 985 185 205 12724159
  16. [18]Liu YC Salamone JD Sachs BD Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats J Neurosci 1997 17 5245 53 9185562 PMC6573297
  17. [19]Powers JB Newman SW Bergondy ML MPOA and BNST lesions in male Syrian hamsters: differential effects on copulatory and chemoinvestigatory behaviors Behav Brain Res 1987 23 181 95 3555537
  18. [21]Numan M Numan M A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats Dev Psychobiol 1996 29 23 51 8719181
  19. [23]Kirkpatrick B Carter CS Newman SW Insel TR Axon-sparing lesions of the medial nucleus of the amygdala decrease affiliative behaviors in the prairie vole (Microtus ochrogaster): behavioral and anatomical specificity Behav Neurosci 1994 108 501 13 7917044
  20. [24]Curtis JT Wang Z Forebrain c-fos expression under conditions conducive to pair bonding in female prairie voles (Microtus ochrogaster) Physiol Behav 2003 80 1 95 101 14568313
  21. [25]Cushing BS Mogekwu N Le WW Hoffman GE Carter CS Cohabitation induced Fos immunoreactivity in the monogamous prairie vole Brain Res 2003 965 203 11 12591139
  22. [26]Kirkpatrick B Kim JW Insel TR Limbic system fos expression associated with paternal behavior Brain Res 1994 658 112 8 7834331
  23. [27]Northcutt KV Lonstein JS Social contact elicits immediate-early gene expression in dopaminergic cells of the male prairie vole extended olfactory amygdala Neuroscience 2009 163 9 22 19524021 PMC2873689
  24. [28]Wang Z Hulihan TJ Insel TR Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles Brain Res 1997 767 321 32 9367264
  25. [29]Young KA Liu Y Wang Z The neurobiology of social attachment: A comparative approach to behavioral, neuroanatomical, and neurochemical studies Comp Biochem Physiol C Toxicol Pharmacol 2008 148 401 10 18417423 PMC2683267
  26. [33]Northcutt KV Wang Z Lonstein JS Sex and species differences in tyrosine hydroxylase-synthesizing cells of the rodent olfactory extended amygdala J Comp Neurol 2007 500 103 15 17099901
  27. [35]Fowler CD Johnson F Wang Z Estrogen regulation of cell proliferation and distribution of estrogen receptor-alpha in the brains of adult female prairie and meadow voles J Comp Neurol 2005 489 166 79 15984004 PMC3962047
  28. [36]Cushing BS Wynne-Edwards KE Estrogen receptor-alpha distribution in male rodents is associated with social organization J Comp Neurol 2006 494 595 605 16374794
  29. [37]Northcutt KV Lonstein JS Sex differences and effects of neonatal aromatase inhibition on masculine and feminine copulatory potentials in prairie voles Horm Behav 2008 54 160 9 18378236 PMC2862256
  30. [38]Swanson LW Brain maps: structure of the rat brain 2nd 1998 Amsterdam Elsevier
  31. [39]Bean NJ Nyby J Kerchner M Dahinden Z Hormonal regulation of chemosignal-stimulated precopulatory behaviors in male housemice (Mus musculus) Horm Behav 1986 20 390 404 3793021
  32. [40]Asmus SE Kincaid AE Newman SW A species-specific population of tyrosine hydroxylase-immunoreactive neurons in the medial amygdaloid nucleus of the Syrian hamster Brain Res 1992 575 199 207 1349252
  33. [41]Asmus SE Newman SW Tyrosine hydroxylase neurons in the male hamster chemosensory pathway contain androgen receptors and are influenced by gonadal hormones J Comp Neurol 1993 331 445 57 8099590
  34. [42]Verney C Gaspar P Febvret A Berger B Transient tyrosine hydroxylase-like immunoreactive neurons contain somatostatin and substance P in the developing amygdala and bed nucleus of the stria terminalis of the rat Brain Res 1988 470 45 58 2457412
  35. [43]Gréco B Edwards DA Michael RP Clancy AN Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express Fos immunoreactivity induced by mating Neuroendocrinology 1998 67 18 28 9485165
  36. [44]Wood RI Newman SW Androgen and estrogen receptors coexist within individual neurons in the brain of the Syrian hamster Neuroendocrinology 1995 62 487 97 8559280
  37. [45]Lansing SW Lonstein JS Tyrosine hydroxylase-synthesizing cells in the hypothalamus of prairie voles (Microtus ochrogaster): sex differences in the anteroventral periventricular preoptic area and effects of adult gonadectomy or neonatal gonadal hormones J Neurobiol 2006 66 197 204 16329116
  38. [46]Foidart A Harada N Balthazart J Aromatase-immunoreactive cells are present in mouse brain areas that are known to express high levels of aromatase activity Cell Tissue Res 1995 280 561 74 7606769
  39. [47]Wagner CK Morrell JI Distribution and steroid hormone regulation of aromatase mRNA expression in the forebrain of adult male and female rats: a cellular-level analysis using in situ hybridization J Comp Neurol 1996 370 71 84 8797158
  40. [48]Cushing BS Perry A Musatov S Ogawa S Papademetriou E Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior J Neurosci 2008 28 10399 403 18842899 PMC2586115
  41. [49]Brawer J Bertley J Beaudet A Testosterone inhibition of tyrosine hydroxylase expression in the hypothalamic arcuate nucleus Neurosci Lett 1986 67 313 8 2874533
  42. [50]Dias BG Ataya RS Rushworth D Zhao J Crews D Effect of incubation temperature and androgens on dopaminergic activity in the leopard gecko, Eublepharis macularius Dev Neurobiol 2007 67 630 6 17443813
  43. [51]Fowler CD Liu Y Ouimet C Wang Z The effects of social environment on adult neurogenesis in the female prairie vole J Neurobiol 2002 51 115 28 11932953
  44. [52]Jeong H Kim MS Kwon J Kim KS Seol W Regulation of the transcriptional activity of the tyrosine hydroxylase gene by androgen receptor Neurosci Lett 2006 396 57 61 16356647
  45. [53]Maharjan S Serova L Sabban EL Transcriptional regulation of tyrosine hydroxylase by estrogen: opposite effects with estrogen receptors alpha and beta and interactions with cyclic AMP J Neurochem 2005 93 1502 14 15935066
  46. [54]Barker JM Galea LA Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats Neuroscience 2008 152 888 902 18353559
  47. [55]Bethea CL Reddy AP Tokuyama Y Henderson JA Lima FB Protective actions of ovarian hormones in the serotonin system of macaques Front Neuroendocrinol 2009 30 212 38 19394356 PMC2704571
  48. [56]Cooke BM Steroid-dependent plasticity in the medial amygdala Neuroscience 2006 138 997 1005 16330154
  49. [57]Gomez DM Newman SW Medial nucleus of the amygdala in the adult Syrian hamster: a quantitative Golgi analysis of gonadal hormonal regulation of neuronal morphology Anat Rec 1991 231 498 509 1793177
  50. [58]Malsbury CW McKay K Neurotrophic effects of testosterone on the medial nucleus of the amygdala in adult male rats J Neuroendocrinol 1994 6 57 69 7517749
  51. [59]Morris JA Jordan CL King ZA Northcutt KV Breedlove SM Sexual dimorphism and steroid responsiveness of the posterodorsal medial amygdala in adult mice Brain Res 2008 1190 115 21 18054901 PMC2258085
  52. [60]De Vries GJ Simerly RB Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain Pfaff DW Arnold AP Etgen AM Fahrbach SE Rubin RT Hormones, Brain and Behavior 4 Elsevier New York 2002 137 191
  53. [62]Klein SL Hairston JE Devries AC Nelson RJ Social environment and steroid hormones affect species and sex differences in immune function among voles Horm Behav 1997 32 30 9 9344689

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Authors
Cavanaugh, B. L., & Lonstein, J. S.
Affiliations
Michigan State University (US)
Corresponding author
Lonstein, J. S.
Venue
Journal of Neuroendocrinology
Publisher
Wiley
Published
2010-03-17
Volume
22
Issue
4
Pages
217-225
ISSN
  • 0953-8194 (ISSN-L)
  • 1365-2826
OpenAlex
W2127313578
Cited by
23
References
8
Citations by year
2025: 2 · 2022: 1 · 2020: 1 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 1 · 2014: 2 · 2013: 1 · 2012: 4
FWCI
5.25
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Mental Health (T32MH070343)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
  • Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Keywords
tyrosine hydroxylase, catecholaminergic neurons, Microtus ochrogaster, medial amygdala, bed nucleus of the stria terminalis, androgen receptor, estrogen receptor alpha, gonadal hormones, testosterone, estradiol benzoate, dihydrotestosterone, castration, ovariectomy, sexual dimorphism
MeSH terms
Amygdala, Androgens, Animals, Castration, Arvicolinae, Drug Implants, Estradiol, Female, Immunohistochemistry, Male, Receptors, Androgen, Septal Nuclei, Dihydrotestosterone, Tyrosine 3-Monooxygenase, Estrogen Receptor alpha, Infusions, Subcutaneous

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