Maternal treatment with fluoxetine promotes testicular alteration in male rat pups
Aline C. Ramos A , Alice H. dos Santos A , Kennia M. Silveira A , Ana Carolina I. Kiss B , Suzana F. P. Mesquita C and Daniela C. C. Gerardin A D
+ Author Affiliations
- Author Affiliations
A Department of Physiological Sciences, State University of Londrina, 86051-980, Londrina, Paraná, Brazil.
B Department of Physiology, São Paulo State University, 18618-970, Botucatu, São Paulo, Brazil.
C Department of Biology, State University of Londrina, 86051-980, Londrina, Paraná, Brazil.
D Corresponding author. Email: dcgerardin@uel.br
Reproduction, Fertility and Development 28(8) 1206-1213 https://doi.org/10.1071/RD14199
Submitted: 11 June 2014 Accepted: 8 December 2014 Published: 13 January 2015
Abstract
Fluoxetine (FLX) is a selective serotonin reuptake inhibitor (SSRI) antidepressant commonly prescribed during pregnancy and lactation. Pre- and post-partum depression, as well as SSRI treatment during these periods, may change maternal care, interfering with offspring development. Moreover, it is known that SSRIs may alter testes structure and function in offspring. The present study investigated the effects of maternal FLX exposure on maternal behaviour and testes function in offspring. Female Wistar rats were treated with 7.5 mg kg–1 FLX or tap water (control group) by gavage from the Day 1 of pregnancy until 21 days after birth (postnatal Day (PND) 21). Maternal behaviour was evaluated and morphofunctional analyses of offspring testes were conducted on PND 21 and 50. There were no significant differences between the FLX-treated and control groups regarding maternal behaviour. Nor did maternal treatment with FLX have any effect on bodyweight gain, anogenital distance, day of preputial separation, testis weight and the gonadosomatic index in male offspring. However, there was a decreased number of Sertoli cells at both PND 21 and 50 in FLX-exposed male offspring. The findings of the present study demonstrate that maternal exposure to FLX can impair testicular function in weanling and pubertal animals.
Additional keywords: antidepressant, maternal behaviour, testes.
References
Abercrombie, M. (1946). Estimation of nuclear populations from microtome sections. Anat. Rec. 94, 239–247.| Estimation of nuclear populations from microtome sections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaH28%2FjtlOisQ%3D%3D&md5=06b1bb3fa91735aee63411b980e067b0CAS | 21015608PubMed |
Aguilar, R., Antón, F., Bellido, C., Aguillar, E., and Gaytan, F. (1995). Testicular serotonin is related to mast cells but not to Leydig cells in the rat. J. Endocrinol. 146, 15–21.
| Testicular serotonin is related to mast cells but not to Leydig cells in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvVylsb0%3D&md5=d3f1e62525da90e50fb2d66246061911CAS | 7561612PubMed |
Amann, R. P., and Almquist, J. O. (1962). Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production. J. Dairy Sci. 45, 774–781.
| Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production.Crossref | GoogleScholarGoogle Scholar |
Attal, J., and Courot, M. (1963). Développement testiculaire et établissement de la spermatogénèse chez le taureau. Ann. Biol. Anim. Biochim. Biophys. 3, 219–241.
| Développement testiculaire et établissement de la spermatogénèse chez le taureau.Crossref | GoogleScholarGoogle Scholar |
Bagdy, G., and Kalogeras, K. T. (1993). Stimulation of 5-HT1A and 5-HT2/5-HT1C receptors induce oxytocin release in the male rat. Brain Res. 611, 330–332.
| Stimulation of 5-HT1A and 5-HT2/5-HT1C receptors induce oxytocin release in the male rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltV2nsLk%3D&md5=248665a6778c67712c343f603ad13760CAS | 8334526PubMed |
Bagdy, G., Kalogeras, K. T., and Szemeredi, K. (1992). Effect of 5-HT1C and 5-HT2 receptor stimulation on excessive grooming, penile erection and plasma oxytocin concentrations. Eur. J. Pharmacol. 229, 9–14.
| Effect of 5-HT1C and 5-HT2 receptor stimulation on excessive grooming, penile erection and plasma oxytocin concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlt12kuw%3D%3D&md5=ce31d827aabd1a21ce0d58f3372715ccCAS | 1:CAS:528:DyaK3sXlt12kuw%3D%3D&md5=ce31d827aabd1a21ce0d58f3372715ccCAS | 1473565PubMed |
Barofsky, A. L., Taylor, J., Tizabi, Y., Kumar, R., and Jones-Quartey, K. (1983). Specific neurotoxin lesions of median raphe serotonergic neurons disrupt maternal behavior in the lactating rat. Endocrinology 113, 1884–1893.
| Specific neurotoxin lesions of median raphe serotonergic neurons disrupt maternal behavior in the lactating rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXmtVKqs7w%3D&md5=7ef2d4e643389937339dbe3ab3847805CAS | 1:CAS:528:DyaL3sXmtVKqs7w%3D&md5=7ef2d4e643389937339dbe3ab3847805CAS | 6685026PubMed |
Bridges, R. S., DiBiase, R., Loundes, D. D., and Doherty, P. C. (1985). Prolactin stimulation of maternal behavior in female rats. Science 227, 782–784.
| Prolactin stimulation of maternal behavior in female rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtVKksbw%3D&md5=f1cd71477b44b91e8654efbc7c8b2ba9CAS | 1:CAS:528:DyaL2MXhtVKksbw%3D&md5=f1cd71477b44b91e8654efbc7c8b2ba9CAS | 3969568PubMed |
Bridges, R. S., Numan, M., Ronshein, P. M., Mann, P. E., and Lupini, C. E. (1990). Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc. Natl Acad. Sci. USA 87, 8003–8007.
| Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXmtVGisL0%3D&md5=fb785a1c6cf2b5c826cc117a6aa4dafaCAS | 2236014PubMed |
Campos, M. B., Vitale, M. L., Calandra, R. S., and Chiochio, S. R. (1990). Serotoninergic innervations of the rat testis. J. Reprod. Fertil. 88, 475–479.
| Serotoninergic innervations of the rat testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslaqsLc%3D&md5=de1670a3c4f903d4e3b7ecc1147e727bCAS | 1:CAS:528:DyaK3cXhslaqsLc%3D&md5=de1670a3c4f903d4e3b7ecc1147e727bCAS | 2325015PubMed |
Cummings, J. A., Clemens, L. G., and Nunez, A. A. (2010). Mother counts: How effects of environmental contaminants on maternal care could affect the offspring and future generations. Front. Neuroendocrinol. 31, 440–451.
| Mother counts: How effects of environmental contaminants on maternal care could affect the offspring and future generations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtleqt7jK&md5=6c090a9d790546c1264d88a93b61f45dCAS | 1:CAS:528:DC%2BC3cXhtleqt7jK&md5=6c090a9d790546c1264d88a93b61f45dCAS | 20685293PubMed |
Das, T. K., Mazunder, R., and Biswas, N. M. (1982). Spermatogenesis in rat: effect of l-tryptophan loading. Andrologia 14, 242–249.
| Spermatogenesis in rat: effect of l-tryptophan loading.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XksFShur4%3D&md5=0bad11733321bae65912ce1ac09d67c8CAS | 1:CAS:528:DyaL38XksFShur4%3D&md5=0bad11733321bae65912ce1ac09d67c8CAS | 6956243PubMed |
Das, T. K., Mazunder, R., and Biswas, N. M. (1985). Effect of intraventricular injection of 5,6-dihydroxytryptamine on spermatogenesis and plasma testosterone levels in rat. J. Endocrinol. 106, 395–400.
| Effect of intraventricular injection of 5,6-dihydroxytryptamine on spermatogenesis and plasma testosterone levels in rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltlGktbo%3D&md5=5e03629eed01b807eee880bad9f5503fCAS | 1:CAS:528:DyaL2MXltlGktbo%3D&md5=5e03629eed01b807eee880bad9f5503fCAS | 4045346PubMed |
de Oliveira, W. M., de Sá, I. R., de Torres, S. M., de Morais, R. N., Andrade, A. M., Maia, F. C., Tenorio, B. M., and da Silva Junior, V. A. (2013). Perinatal exposure to fluoxetine via placenta and lactation inhibits the testicular development in male rat offspring. Syst. Biol. Reprod. Med. 59, 244–250.
| Perinatal exposure to fluoxetine via placenta and lactation inhibits the testicular development in male rat offspring.Crossref | GoogleScholarGoogle Scholar | 23651434PubMed |
Deiró, T. C. B. J., Manhães de Castro, R., Cabral Filho, J. E., Souza, S. L., Freitas, S., Ferreira, L. M. P., Guedes, R. C. A., Câmara, C. R. V., and Barros, K. M. F. T. (2004). Neonatal administration of citalopram delays somatic maturation in rats. Braz. J. Med. Biol. Res. 37, 1503–1509.
| Neonatal administration of citalopram delays somatic maturation in rats.Crossref | GoogleScholarGoogle Scholar |
Dorst, V. J., and Sajonski, H. (1974). Morphometrische untersuchunhen am tubulussystem des schweinehodens während der postnatalen entwicklug. Monotsh. Ver. Med. 29, 650–652.
Ferreira, A., Picazo, O., Uriarte, N., Pereira, M., and Fernandez-Guasti, A. (2000). Inhibitory effect of buspirone and diazepam, but not of 8-OH-DPAT, on maternal behavior and aggression. Pharmacol. Biochem. Behav. 66, 389–396.
| Inhibitory effect of buspirone and diazepam, but not of 8-OH-DPAT, on maternal behavior and aggression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFersLo%3D&md5=7545c76b227d6bad0132b30200024aebCAS | 1:CAS:528:DC%2BD3cXksFersLo%3D&md5=7545c76b227d6bad0132b30200024aebCAS | 10880695PubMed |
Ferris, C., Foote, K., Meltser, H., Plenby, M., Smith, K., and Insel, T. (1992). Oxytocin in the amygdala facilitates maternal aggression. In ‘Oxytocin and Maternal Sexual and Social Behaviors’. Vol. 474. (Eds C. A. Pedersen, J. D. Caldwell, J. D. Jirikowski and T. R. Insel.) pp. 226–33. (New York Academy of Sciences: New York.)
Ferro, T., Verdeli, H., Pierre, F., and Weissman, M. M. (2000). Screening for depression in mothers bringing their offspring for evaluation or treatment of depression. Am. J. Psychiatry 157, 375–379.
| Screening for depression in mothers bringing their offspring for evaluation or treatment of depression.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7mtl2gtg%3D%3D&md5=ce8b23f0660be39539c5f25687c2bea6CAS | 1:STN:280:DC%2BD3c7mtl2gtg%3D%3D&md5=ce8b23f0660be39539c5f25687c2bea6CAS | 10698812PubMed |
França, L. R., and Cardoso, F. M. (1998). Duration of spermatogenesis and sperm transit time through the epididymis in the piau boar. Tissue Cell 30, 573–582.
| Duration of spermatogenesis and sperm transit time through the epididymis in the piau boar.Crossref | GoogleScholarGoogle Scholar | 9839480PubMed |
França, L. R., and Russell, L. D. (1998). The testes of domestic mammals. In ‘Male Reproduction: A Multidisciplinary Overview’. (Eds F. Martinez-Garcia and J. Regadera.) pp. 197–219. (Churchill Communications: Madrid.)
Gaffori, O., and Le Moal, M. (1979). Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmentum lesions. Physiol. Behav. 23, 317–323.
| Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmentum lesions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c%2Flslahtw%3D%3D&md5=7e98cba5a68862f7e1db27cc3259df07CAS | 1:STN:280:DyaL3c%2Flslahtw%3D%3D&md5=7e98cba5a68862f7e1db27cc3259df07CAS | 504422PubMed |
Gore, A. C. (2001). Environmental toxicant effects on neuroendocrine function. Endocrine 14, 235–246.
| Environmental toxicant effects on neuroendocrine function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFantLY%3D&md5=ed5a8af452da71dbbb148c028d14e411CAS | 1:CAS:528:DC%2BD3MXjvFantLY%3D&md5=ed5a8af452da71dbbb148c028d14e411CAS | 11394642PubMed |
Griswold, M. D. (1998). The central role of Sertoli cells in spermatogenesis. Semin. Cell Dev. Biol. 9, 411–416.
| The central role of Sertoli cells in spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFyl&md5=171e22e4b3599291d36c604081bff1e6CAS | 1:CAS:528:DyaK1MXlvFyl&md5=171e22e4b3599291d36c604081bff1e6CAS | 9813187PubMed |
Hansen, S. (1994). Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit. Physiol. Behav. 55, 615–620.
| Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3kvVajug%3D%3D&md5=41b0fdc120733e0f6566fb2686ea68f8CAS | 1:STN:280:DyaK2c3kvVajug%3D%3D&md5=41b0fdc120733e0f6566fb2686ea68f8CAS | 8190785PubMed |
Hendrick, V., Stowe, Z. N., Altshuler, L. L., Mintz, J., Hwang, S., Hostetter, A., Suri, R., Leight, K., and Fukuchi, A. (2001). Fluoxetine and norfluoxetine concentrations in nursing infants and breast milk. Biol. Psychiatry 50, 775–782.
| Fluoxetine and norfluoxetine concentrations in nursing infants and breast milk.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosFKksr0%3D&md5=e39dd5e687a82afce77709fc54dbb866CAS | 1:CAS:528:DC%2BD3MXosFKksr0%3D&md5=e39dd5e687a82afce77709fc54dbb866CAS | 11720696PubMed |
Hochereu-de Reviers, M. T., and Lincoln, G. A. (1978). Seasonal variation in the histology of the testes of the red deer, Cervus elaphus. J. Reprod. Fertil. 54, 209–213.
| Seasonal variation in the histology of the testes of the red deer, Cervus elaphus.Crossref | GoogleScholarGoogle Scholar |
Hooley, R. P., Paterson, M., Brown, P., Kerr, K., and Saunders, P. T. K. (2009). Intra-testicular injection of adenoviral constructs results in Sertoli cell-specific gene expression and disruption of seminiferous epithelium. Reproduction 137, 361–370.
| Intra-testicular injection of adenoviral constructs results in Sertoli cell-specific gene expression and disruption of seminiferous epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ksb8%3D&md5=6fc426482b26bc2e8acd1c55bb9d8431CAS | 1:CAS:528:DC%2BD1MXovV2ksb8%3D&md5=6fc426482b26bc2e8acd1c55bb9d8431CAS | 18955374PubMed |
Johns, J. M., Faggin, B. M., Noonan, L. R., Li, L., Zimmerman, L. I., and Pedersen, C. A. (1995). Chronic cocaine treatment decreases oxytocin levels in the amygdala and increases maternal aggression in Sprague-Dawley rats. Society for Neuroscience Abstracts 21, 766.7.
Johns, J. M., Lubin, D. A., Walker, C. H., Meter, K. E., and Mason, G. A. (1997). Chronic gestational cocaine treatment decreases oxytocin levels in the medial preoptic area, ventral tegmental area and hippocampus in Sprague-Dawley rats. Neuropeptides 31, 439–443.
| Chronic gestational cocaine treatment decreases oxytocin levels in the medial preoptic area, ventral tegmental area and hippocampus in Sprague-Dawley rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvF2mtrg%3D&md5=c8bdc866b3257750b5da162c5ae2baf5CAS | 1:CAS:528:DyaK2sXnvF2mtrg%3D&md5=c8bdc866b3257750b5da162c5ae2baf5CAS | 9413020PubMed |
Johns, J. M., Elliott, D. L., Hofler, V. E., Joyner, P. W., McMurray, M. S., Jarrett, T. M., Haslup, A. M., Middleton, C. L., Elliott, J. C., and Walker, C. H. (2005a). Cocaine treatment and prenatal environment interact to disrupt intergenerational maternal behavior in rats. Behav. Neurosci. 119, 1605–1618.
| Cocaine treatment and prenatal environment interact to disrupt intergenerational maternal behavior in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhtl2lt7Y%3D&md5=b5d5eaca9babe46688303444378352a0CAS | 1:CAS:528:DC%2BD28Xhtl2lt7Y%3D&md5=b5d5eaca9babe46688303444378352a0CAS | 16420163PubMed |
Johns, J. M., Joyner, P. W., McMurray, M. S., Elliott, D. L., Hofler, V. E., Middleton, C. L., Knupp, K., Greenhill, K. W., Lomas, L. M., and Walker, C. H. (2005b). The effects of dopaminergic/serotonergic reuptake inhibition on maternal behavior, maternal aggression, and oxytocin in the rat. Pharmacol. Biochem. Behav. 81, 769–785.
| The effects of dopaminergic/serotonergic reuptake inhibition on maternal behavior, maternal aggression, and oxytocin in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXos1WrtLg%3D&md5=07185b2c26f1360ee9261d3fb9e2f066CAS | 1:CAS:528:DC%2BD2MXos1WrtLg%3D&md5=07185b2c26f1360ee9261d3fb9e2f066CAS | 15996723PubMed |
Kaffman, A., and Meaney, M. J. (2007). Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. J. Child Psychol. Psychiatry 48, 224–244.
| Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights.Crossref | GoogleScholarGoogle Scholar | 17355397PubMed |
Kessler, R. C., McGonagle, K. A., Swartz, M., Blazer, D. G., and Nelson, C. B. (1993). Sex and depressionin the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence. J. Affect. Disord. 29, 85–96.
| Sex and depressionin the National Comorbidity Survey. I: lifetime prevalence, chronicity and recurrence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7jt1Cmsg%3D%3D&md5=c21ce4c335b3a80456649df39e4af254CAS | 1:STN:280:DyaK2c7jt1Cmsg%3D%3D&md5=c21ce4c335b3a80456649df39e4af254CAS | 8300981PubMed |
Kimble, D. P., Rogers, L., and Hendrickson, C. W. (1967). Hippocampal lesions disrupt maternal, not sexual behavior in the albino rat. J. Comp. Physiol. Psychol. 63, 401–407.
| Hippocampal lesions disrupt maternal, not sexual behavior in the albino rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1c%2FosVylsg%3D%3D&md5=58113ee96a335f98578115eec0a47499CAS | 1:STN:280:DyaF1c%2FosVylsg%3D%3D&md5=58113ee96a335f98578115eec0a47499CAS | 6064383PubMed |
Kiss, A. C., Woodside, B., Felício, L. F., Anselmo-Franci, J., and Damasceno, D. C. (2012). Impact of maternal mild hyperglycemia on maternal care and offspring development and behavior of Wistar rats. Physiol. Behav. 107, 292–300.
| Impact of maternal mild hyperglycemia on maternal care and offspring development and behavior of Wistar rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCkt7nO&md5=273cb7bca079f94a09ba28fa8b280474CAS | 1:CAS:528:DC%2BC38XhslCkt7nO&md5=273cb7bca079f94a09ba28fa8b280474CAS | 22892541PubMed |
Lerch-Haner, J. K., Frierson, D., Crawford, L. K., Beck, S. G., and Deneris, E. S. (2008). Serotonergic transcriptional programming determines maternal behavior and offspring survival. Nat. Neurosci. 11, 1001–1003.
| Serotonergic transcriptional programming determines maternal behavior and offspring survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVamurrO&md5=4bb4b5f86336e4159dd34796230f83fcCAS | 1:CAS:528:DC%2BD1cXhtVamurrO&md5=4bb4b5f86336e4159dd34796230f83fcCAS | 19160496PubMed |
Li, S., and Pelletier, G. (1995). Involvement of serotonin in the regulation of GnRH gene expression in the male rat brain. Neuropeptides 29, 21–25.
| Involvement of serotonin in the regulation of GnRH gene expression in the male rat brain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsVygur8%3D&md5=06eb4534ac5c6947e095e95072ead17cCAS | 1:CAS:528:DyaK2MXnsVygur8%3D&md5=06eb4534ac5c6947e095e95072ead17cCAS | 7566509PubMed |
Lisboa, S. F. S., Oliveira, P. E., Costa, L. C., Venâncio, E. J., and Moreira, E. G. (2007). Behavioral evaluation of male and female mice pups exposed to fluoxetine during pregnancy and lactation. Pharmacology 80, 49–56.
| Behavioral evaluation of male and female mice pups exposed to fluoxetine during pregnancy and lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntVSlt7g%3D&md5=e545850d7ab8c47bc9324572fb0b372bCAS | 1:CAS:528:DC%2BD2sXntVSlt7g%3D&md5=e545850d7ab8c47bc9324572fb0b372bCAS |
Liu, J., and Lauder, J. M. (1992). Serotonin promotes region-specific glial influences on cultures serotonin and dopamine neurons. Glia 5, 306–317.
| Serotonin promotes region-specific glial influences on cultures serotonin and dopamine neurons.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK383mslGqtQ%3D%3D&md5=eb37bb63f87373ae2ae7456c29b88354CAS | 1:STN:280:DyaK383mslGqtQ%3D%3D&md5=eb37bb63f87373ae2ae7456c29b88354CAS | 1350272PubMed |
Lonstein, J. S., Simmons, D. A., Swann, J. M., and Stern, J. M. (1997). Forebrain expression of c-fos due to active maternal behaviour in lactating rats. Neuroscience 82, 267–281.
| Forebrain expression of c-fos due to active maternal behaviour in lactating rats.Crossref | GoogleScholarGoogle Scholar |
Lubin, D. A., Elliot, J. C., Black, M. C., and John, J. M. (2003). An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav. Neurosci. 117, 195–201.
| An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFehsbw%3D&md5=9a5cbf6ce12b8542a41f95ad6a9253cfCAS | 1:CAS:528:DC%2BD3sXivFehsbw%3D&md5=9a5cbf6ce12b8542a41f95ad6a9253cfCAS | 12708515PubMed |
Naumenko, E. V., and Shishkina, G. T. (1978). Role of serotonin in feedback control of hypothalamic–pituitary–testicular complex in male rat. Neuroendocrinology 26, 359–366.
| Role of serotonin in feedback control of hypothalamic–pituitary–testicular complex in male rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXltVCqsr0%3D&md5=1587e53b524c8abf413c7a27f246958eCAS | 1:CAS:528:DyaE1cXltVCqsr0%3D&md5=1587e53b524c8abf413c7a27f246958eCAS | 151240PubMed |
Nissen, E., Gustavsson, P., Widstrom, A. M., and Uvnas-Moberg, K. (1998). Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or cesareansection. J. Psychosom. Obstet. Gynaecol. 19, 49–58.
| Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or cesareansection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3js1ersA%3D%3D&md5=3849f7ed4cfbfe8c8a64585f332e376bCAS | 1:STN:280:DyaK1c3js1ersA%3D%3D&md5=3849f7ed4cfbfe8c8a64585f332e376bCAS | 9575469PubMed |
Numan, M. (1994a). A neural circuitry analysis of maternal behavior in the rat. Acta Paediatr. Suppl. 83, 19–28.
| A neural circuitry analysis of maternal behavior in the rat.Crossref | GoogleScholarGoogle Scholar |
Numan, M. (1994b). Maternal behavior. In ‘The Physiology Of Reproduction 2’. (Eds E. Knobil and J. D. Neill.) pp. 221–301. (Raven Press: New York.)
Numan, M., and Smith, H. G. (1984). Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 98, 712–727.
| Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c3otVeqtQ%3D%3D&md5=d1386f01f88de745afd838691bcee713CAS | 6087844PubMed |
Orth, J. M. (1982). Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat. Rec. 203, 485–492.
| Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2Fks1eqsg%3D%3D&md5=abded53ce2e8ce4cbf8f87761923db1dCAS | 7137603PubMed |
Orth, J. M., Gunsalus, G. L., and Lamperti, A. A. (1988). Evidence from Sertoli cell depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 122, 787–794.
| Evidence from Sertoli cell depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7jslWgug%3D%3D&md5=14acf24f80c90bf4cf7778b3b5c7d86cCAS | 1:STN:280:DyaL1c7jslWgug%3D%3D&md5=14acf24f80c90bf4cf7778b3b5c7d86cCAS | 3125042PubMed |
Ottoni, E. B. (2000). EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behav. Res. Methods Instrum. Comput. 32, 446–449.
| EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvnvV2kug%3D%3D&md5=09bdbcb1e182da0464d4e363dd906d2dCAS | 1:STN:280:DC%2BD3cvnvV2kug%3D%3D&md5=09bdbcb1e182da0464d4e363dd906d2dCAS | 11029818PubMed |
Palén, K., Thörneby, L., and Emanuelsson, H. (1979). Effects of serotonin and serotonin antagonists on chick embryogenesis. Wilhelm Roux’s Archives of Developmental Biology 187, 89–103.
| Effects of serotonin and serotonin antagonists on chick embryogenesis.Crossref | GoogleScholarGoogle Scholar |
Pawluski, J. L., Charlier, T., Fillet, M., Houbart, V., Crispin, H. T., Steinbusch, H. W., and Van den Hove, D. L. (2012). Chronic fluoxetine treatment and maternal adversity differentially alter neurobehavioral outcomes in the rat dam. Behav. Brain Res. 228, 159–168.
| Chronic fluoxetine treatment and maternal adversity differentially alter neurobehavioral outcomes in the rat dam.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht12jsr8%3D&md5=d8996c4872fedef59b46426b914fe6eaCAS | 1:CAS:528:DC%2BC38Xht12jsr8%3D&md5=d8996c4872fedef59b46426b914fe6eaCAS | 22173000PubMed |
Pohland, R. C., Byrd, T. K., Hamilton, M., and Koons, J. R. (1989). Placental transfer and fetal distribution of fluoxetine in the rat. Toxicol. Appl. Pharmacol. 98, 198–205.
| Placental transfer and fetal distribution of fluoxetine in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktVSisbs%3D&md5=a4e0d6c2f424dcb3b9b1b603462b92d1CAS | 1:CAS:528:DyaL1MXktVSisbs%3D&md5=a4e0d6c2f424dcb3b9b1b603462b92d1CAS | 2785300PubMed |
Saydoff, J. A., Rittenhouse, P. A., Van De Kar, L. D., and Brownfield, M. S. (1991). Enhanced serotonergic transmission stimulates oxytocin secretion in conscious male rats. J. Pharmacol. Exp. Ther. 257, 95–99.
| 1:CAS:528:DyaK3MXit1Wks7w%3D&md5=ee75b9692a6ec1fdae4849c48cc11d7bCAS |
| 1:CAS:528:DyaK3MXit1Wks7w%3D&md5=ee75b9692a6ec1fdae4849c48cc11d7bCAS | 1850481PubMed |
Silva, J. V. A., Lins, A. M. J. A. A., Amorim, J. A. A., Pinto, C. F., Deiró, T. B. J., Oliveira, J. R. M., Peixoto, C. A., and Manhães-de-Castro, R. (2008). Neonatal administration of fluoxetine decreased final sertoli cell number in Wistar rats. Int. J. Morphol. 26, 51–62.
Strathearn, L., and Mayes, L. C. (2010). Cocaine addiction in mothers: potential effects on maternal care and infant development. Ann. N. Y. Acad. Sci. 1187, 172–183.
| Cocaine addiction in mothers: potential effects on maternal care and infant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Smsrw%3D&md5=4ec4b0313d13118be48b6583d48c66e7CAS | 1:CAS:528:DC%2BC3cXks1Smsrw%3D&md5=4ec4b0313d13118be48b6583d48c66e7CAS | 20201853PubMed |
Syed, V., Gomez, E., and Hecht, N. B. (1999). Messenger ribonucleic acids encoding a serotonin receptor and a novel gene are induced in Sertoli cells by a secreted factor(s) from male rat meiotic germ cells. Endocrinology 140, 5754–5760.
| 1:CAS:528:DyaK1MXns12htLs%3D&md5=9557e9a04396f37e500535dae2f7110aCAS |
| 1:CAS:528:DyaK1MXns12htLs%3D&md5=9557e9a04396f37e500535dae2f7110aCAS | 10579341PubMed |
Tinajero, J. C., Fabbri, A., and Dufau, M. L. (1993). Serotonergic inhibition of rat Leydig cell function by propanolol. Endocrinology 133, 257–264.
| 1:CAS:528:DyaK3sXlsFWrurg%3D&md5=1f666d437b8c63c87e77528b0be67841CAS |
| 1:CAS:528:DyaK3sXlsFWrurg%3D&md5=1f666d437b8c63c87e77528b0be67841CAS | 8391422PubMed |
Urry, R. L., and Dougherty, M. S. (1975). Inhibition of rat spermatogenesis and seminiferous tubule growth after short-term and long-term administration of a monoamine oxidase inhibitor. Fertil. Steril. 26, 232–239.
| 1:STN:280:DyaE2M7ht1CrtA%3D%3D&md5=6535b03d3df782adfead3f98945ee07eCAS |
| 1:STN:280:DyaE2M7ht1CrtA%3D%3D&md5=6535b03d3df782adfead3f98945ee07eCAS | 1116620PubMed |
Uvnäs-Moberg, K., Hillegaart, V., Alster, P., and Ahlenius, S. (1996). Effects of 5-HT agonists, selective for different receptor subtypes, on oxytocin, CCK, gastrin and somatostatin plasma levels in the rat. Neuropharmacology 35, 1635–1640.
| Effects of 5-HT agonists, selective for different receptor subtypes, on oxytocin, CCK, gastrin and somatostatin plasma levels in the rat.Crossref | GoogleScholarGoogle Scholar | 9025112PubMed |
Vieira, M. L., dos Santos, A. H., Silva, L. S., Fernandes, G. S., Kiss, A. C., Moreira, E. G., Mesquita, S. F., and Gerardin, D. C. (2013a). Lactational exposure to sulpiride: assessment of maternal care and reproductive and behavioral parameters of male rat pups. Physiol. Behav. 122, 76–83.
| Lactational exposure to sulpiride: assessment of maternal care and reproductive and behavioral parameters of male rat pups.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVWlu7nF&md5=fd2ac48da92d2c411d7bf36c0533fea3CAS | 1:CAS:528:DC%2BC3sXhvVWlu7nF&md5=fd2ac48da92d2c411d7bf36c0533fea3CAS | 24021925PubMed | 24021925PubMed |
Vieira, M. L., Hamada, R. Y., Gonzaga, N. I., Bacchi, A. D., Barbieri, M., Moreira, E. G., Mesquita, S. F. P., and Gerardin, D. C. C. (2013b). Could maternal exposure to the antidepressants fluoxetine and St. John’s wort induce long-term reproductive effects on male rats? Reprod. Toxicol. 35, 102–107.
| Could maternal exposure to the antidepressants fluoxetine and St. John’s wort induce long-term reproductive effects on male rats?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFGisbrO&md5=19cccd3c6ab28c122f62b177c9fcaa1eCAS | 1:CAS:528:DC%2BC38XhtFGisbrO&md5=19cccd3c6ab28c122f62b177c9fcaa1eCAS | 22824787PubMed | 22824787PubMed |
Weissman, M. M., Warner, V., Wick-Ramaratne, P., and Prusoff, B. A. (1988). Early-onset major depression in parents and their children. J. Affect. Disord. 15, 269–277.
| Early-onset major depression in parents and their children.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7gvFOqsg%3D%3D&md5=fbdcf57d320a9d15410f1c9bd700be53CAS | 1:STN:280:DyaL1M7gvFOqsg%3D%3D&md5=fbdcf57d320a9d15410f1c9bd700be53CAS | 2975299PubMed | 2975299PubMed |
Whitaker-Azmitia, P. M. (1991). Role of serotonin and other neurotransmitter receptors in brain development: basis for developmental pharmacology. Pharmacol. Rev. 43, 553–561.
| 1:CAS:528:DyaK38XhsVeqtbY%3D&md5=18fce8246903788b63a1b0eb1ec03e54CAS |
| 1:CAS:528:DyaK38XhsVeqtbY%3D&md5=18fce8246903788b63a1b0eb1ec03e54CAS | 1663620PubMed | 1663620PubMed |
Yan, W., Wilson, C. C., and Haring, J. H. (1997). 5-HT1A receptors mediate the neurotrophic effect of serotonin on developing dentate granule cells. Brain Res. Dev. Brain Res. 98, 185–190.
| 5-HT1A receptors mediate the neurotrophic effect of serotonin on developing dentate granule cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsVemtA%3D%3D&md5=cdaf761284aee4f73f47f65378070e39CAS | 1:CAS:528:DyaK2sXmsVemtA%3D%3D&md5=cdaf761284aee4f73f47f65378070e39CAS | 9051259PubMed | 9051259PubMed |
Yang, Z. W., Wreford, N. G., and de Kretser, D. M. (1990). Quantitative study of spermatogenesis in developing rat testis. Biol. Reprod. 43, 629–635.
| Quantitative study of spermatogenesis in developing rat testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7ksFGgsw%3D%3D&md5=f6b6173a0f9302a70f421924fca6d645CAS | 1:STN:280:DyaK3M7ksFGgsw%3D%3D&md5=f6b6173a0f9302a70f421924fca6d645CAS | 2289015PubMed | 2289015PubMed |
