Electroencephalographic changes and testosterone levels in a pubertal stress animal model: effects on adult sexual motivation

Marisela Hernández González, Enrique Hernández Arteaga, Miguel Ángel Guevara, Herlinda Bonilla Jaime, Marcela Arteaga Silva

DOI: https://doi.org/10.17711/SM.0185-3325.2020.003


Introduction. Stress during puberty exerts long-term effects on endocrine systems and brain structures, such as the prefrontal cortex (PFC) and basolateral amygdala (BLA), two cerebral areas that participate in modulating sexual behavior and whose functioning is regulated by androgenic hormones.

Objective. To evaluate the effect of pubertal stress due to social isolation on the sexual motivation, serum testosterone levels, and electroencephalographic activity (EEG) of the PFC and BLA in male rats.

Method. Sixty sexually-experienced male rats were used. Thirty were stressed by social isolation during puberty (SG, housed 1 per cage, postnatal days 25-50); the other 30 formed the control group (CG, 5 per cage). All rats were implanted bilaterally with stainless steel electrodes in the PFC and BLA. EEGs were recorded during the awake-quiet state in two conditions: without sexual motivation (WSM), and with sexual motivation (SM). After EEG recording, the rats were sacrificed by decapitation to measure their testosterone levels.

Results. SG showed lower sexual motivation and testosterone levels, but higher amygdaline EEG activation in the presence of a receptive female, while CG showed higher prefrontal EEG activation.

Discussion and conclusion. It is probable that the decreased testosterone levels resulting from pubertal stress affected prefrontal and amygdaline functionality and, hence, sexual motivation. These data could explain some of the hormonal and cerebral changes associated with stress-induced sexual alterations, though this suggestion requires additional clinical and animal research.


Stress; social isolation; EEG; testosterone; sexual motivation; rats

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Ågmo, A. (1999). Sexual motivation – an inquiry into events determining the occurrence of sexual behavior. Behavioural Brain Research, 105(1), 129-150. doi: 10.1016/S0166-4328(99)00088-1

Ågmo, A. (2017). ¿Tienen los estudios psicobiológicos, en animales no humanos, alguna relevancia para la conducta humana? El caso de la conducta sexual. In A. C. Medina-Fragoso, M. Hernández-González, C. Amezcua-Gutiérrez, & M. A. Guevara (Eds.), Psicobiología conductual y cognitiva. (pp. 29-51). México: Universidad Nacional Autónoma de México.

Ågmo, A., Villalpando, A., Picker, Z., & Fernández, H. (1995). Lesions of the medial prefrontal cortex and sexual behavior in the male rat. Brain Research, 696(1-2), 177-186. doi: 10.1016/0006-8993(95)00852-H

Ågmo, A., Turi, A. L., Ellingsen, E., & Karpersen, H. (2004). Preclinical models of sexual desire: conceptual and behavioral analyses. Pharmacology, Biochemistry, and Behavior, 78(3), 379-404. doi: 10.1016/j.pbb.2004.04.013

Amistislavskaya, T. G., Bulygina, V. V., Tikhonova, M. A., & Maslova, L. N. (2013). Social isolation during peri-adolescence or adulthood: effects on sexual motivation, testosterone, and corticosterone response under conditions of sexual arousal in male rats. Chinese Journal of Physiology, 56(1), 36-43. doi: 10.4077/CJP.2013.BAA074

Arteaga-Silva, M., Vigueras Villaseñor, R. M., Retana Márquez, S., Hernández González, M., Bonilla Jaime, H., Guzmán García, X., & Contreras Montiel, J. L. (2013). Testosterone levels and development of the penile spines and testicular tissue during the postnatal growth in wistar rats. Advances in Sexual Medicine, 3(3), 1-9. doi: 10.4236/asm.2013.33A001

Balthazart, J., Baillien, M., Cornil, C. A., & Ball, G. F. (2004). Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiology & Behavior, 83(2), 247-270. doi: 10.1016/j.physbeh.2004.08.025

Balthazart, J., Castagna, C., & Ball, G. F. (1997). Differential effects of D1 and D2 dopamine-receptor agonists and antagonists on appetitive and consumatory aspects of male sexual behavior in Japanese quail. Physiology & Behavior, 62(3), 571-580. doi: 10.1016/S0031-9384(97)00163-7

Başar, E., Başar-Eroğlu, C., Karakaş, S., & Schürmann, M. (2000). Brain oscillations in perception and memory. International Journal of Psychophysiology, 35(2-3), 95-124. doi: 10.1016/S0167-8760(99)00047-1

Bland, B. H., & Whishaw, I. Q. (1976). Generators and topography of hippocampal Theta (RSA) in the anesthetized and freely moving rat. Brain Research, 118(2), 259-280. doi: 10.1016/0006-8993(76)90711-3

Bodenmann, G., Ledermann, T., & Bradbury, T. N. (2007). Stress, sex and satisfaction in marriage. Personal Relationship, 14(4), 551-569. doi: 10.1111/j.1475-6811.2007.00171.x

Bodenmann, G., Ledermann, T., Blattner, D., & Galluzo, C. (2006). Associations among everyday stress, critical life events, and sexual problems. The Journal of Nervous and Mental Disease, 194(7), 494-501. doi: 10.1097/01.nmd.0000228504.15569.b6

Bonilla-Jaime, H., Vázquez-Palacios, G., Arteaga-Silva, M., & Retana-Márquez, S. (2006). Hormonal responses to different sexually related conditions in male rats. Hormones & Behavior, 49(3), 376-382. doi: 10.1016/j.yhbeh.2005.08.005

Byun, J. S., Lyu, S. W., Seok, H. H., Kim, W. J, Shim, S. H., & Bak, C. W. (2013). Sexual dysfunctions induced by stress of timed intercourse and medical treatment. British Journal of Urology International, 111(4b), E227-E234. doi: 10.1111/j.1464-410X.2012.11577.x

Cahill, L., & McGaugh, J. L. (1991). NMDA-induced lesions of the amygdaloid complex block the retention-enhancing effect of posttraining epinephrine. Psychobiology, 19(3), 206-210. doi: 10.3758/BF03332069

Cooke, B. M., Chowanadisai, W., & Breedlove, S. M. (2000). Post-weaning social isolation of male rats reduces the volume of the medial amygdala and leads to deficits in adult sexual behavior. Behavioural Brain Research, 117(1-2), 107-113. doi: 10.1016/S0166-4328(00)00301-6

Cunningham, M. G., Bhattacharyya, S., & Benes, F. M. (2002). Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. The Journal of Comparative Neurology, 453(2), 116-130. doi: 10.1002/cne.10376

del Río-Portilla, I., Ugalde, E., Juárez, J., Roldán, A., & Corsi-Cabrera, M. (1997). Sex differences in EEG in adult gonadectomized rats before and after hormonal treatment. Psychoneuroendocrinology, 22(8), 627-642. doi: 10.1016/S0306-4530(97)00056-5

Di Prisco, C. L., Lucarini, N., & Dessì-Fulgheri, F. (1978). Testosterone aromatization in rat brain is modulated by social environment. Physiology & Behavior, 20(3), 345-348. doi: 10.1016/0031-9384(78)90230-5

Djouma, E., Card, K., Lodge, D. J., & Lawrence, A. J. (2006). The CRF1 receptor antagonist, antalarmin, reverses isolation-induced up-regulation of dopamine D2 receptors in the amygdala and nucleus accumbens of fawn-hooded rats. European Journal of Neuroscience, 23(12), 3319-3327. doi: 10.1111/j.1460-9568.2006.04864.x

Duffy, J. A., & Hendricks, S. E. (1973). Influences of social isolation during development on sexual behavior of the rat. Animal Learning and Behavior, 1(3), 223-227. doi: 10.3758/BF03199079

Engel, A., & Singer, W. (2001). Temporal binding and the neural correlates of sensory awareness. Trends in Cognitive Sciences, 5(1), 16-25. doi: 10.1016/S1364-6613(00)01568-0

Fanselow, M. S., & LeDoux, J. E. (1999). Why we think plasticity underlying pavlovian fear conditioning occurs in the basolateral amygdala. Neuron, 23(2), 229-232. doi: 10.1016/s0896-6273(00)80775-8

Fernández-Guasti, A., Omaña-Zapata, I., Luján, M., & Condés-Lara, M. (1994). Actions of sciatic nerve ligature on sexual behavior of sexually experienced and inexperienced male rats: Effects of frontal pole decortication. Physiology & Behavior, 55(3), 577-581. doi: 10.1016/0031-9384(94)90119-8

Gerall, H. D., Ward, I. L., & Gerall, A. A. (1967). Disruption of the male rat’s sexual behavior induced by social isolation. Animal Behaviour, 15(1), 54-58. doi: 10.1016/S0003-3472(67)80010-1

Hernández-Arteaga, E., Hernández-González, M., Ramírez-Rentería, M. L., Almanza-Sepúlveda, M. L., Guevara, M. A., Silva, M. A., & Jaime, H. B. (2016). Prenatal stress alters the developmental pattern of behavioral indices of sexual maturation and copulation in male rats. Physiology & Behavior, 163, 251-257. doi: 10.1016/j.physbeh.2016.05.008

Hernández-González, M. (2000). Prepubertal genital grooming and penile erection in relation to sexual behavior of rats. Physiology & Behavior, 71(1-2), 51-56. doi: 10.1016/S0031-9384(00)00320-6

Hernández-González, M., Guevara, M. A., & Ågmo, A. (2014a). Electroencephalographic activity during sexual behavior: a novel approach to the analysis of drug effects on arousal and motivation relevant for sexual dysfunctions. Pharmacology, Biochemestry, and Behavior, 121, 158-169. doi: 10.1016/j.pbb.2014.02.003

Hernández-González, M., Guevara, M. A., Cervantes, M., Morali G., & Corsi-Cabrera, M. (1998). Characteristic frecuency bands of the cortico-frontal EEG during the sexual interaction of the male rat as a result of factorial analysis. Journal of Physiology-Paris, 92(1), 43-50. doi: 10.1016/S0928-4257(98)80022-3

Hernández-González, M., Guevara, M. A., Ramírez-Rentería, M. L., & Hernández-Arteaga, E. (2015). Post-weaning social isolation alters the development of behavioral indices of sexual maturation and leads to deficits in the sexual behavior of male rats. E-CUCBA, 3, 55-71. doi: 10.32870/e-cucba.v0i3.32

Hernández-González, M., Hernández-Arteaga, E., Guevara, M. A., Almanza-Sepúlveda, M. L., Ramírez-Rentería, M. L., Arteaga-Silva, M., & Bonilla-Jaime, H. (2017). Prenatal stress supresses the prefrontal and amygdaline EEG changes associated with a sexually-motivated state in male rats. Physiology & Behavior, 182(1), 86-92. doi: 10.1016/j.physbeh.2017.10.003

Hernández-González, M., Prieto-Beracoechea, C. A., Arteaga-Silva, M., & Guevara, M. A. (2007). Different functionality of the medial and orbital prefrontal cortex during a sexually motivated task in rats. Physiology & Behavior, 90(2-3), 450-458. doi: 10.1016/j.physbeh.2006.10.006

Hernández-González, M., Robles Aguirre, F. A., Guevara, M. A., Quirarte, G. L., & Haro-Magallanes, P. (2014b). Basolateral Amygdala inactivation reduces sexual motivation in male rats during performance of a T-maze task with a sexual reward. Journal of Behavioral and Brain Science, 4(5), 223-233. doi: 10.4236/jbbs.2014.45024

Joëls, M. (1997). Steroid hormone and excitability in the mammalian brain. Frontiers in Neuroendocrinology, 18(1), 2-48. doi: 10.1006/frne.1996.0144

Kraus, J., Frick, A., Fischer, H., Howner, K., Fredrikson, M., & Furmark, T. (2018). Amygdala reactivity and connectivity during social and non-social aversive stimulation in social anxiety disorder. Psychiatry Research: Neuroimaging, 280, 56-61. doi: 10.1016/j.pscychresns.2018.08.012

Lapiz, M. D. S., Fulford, A., Muchimapura, S., Mason, R., Parker, T., & Marsden, C. A. (2003). Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neuroscience and Behavioral Physiology, 33(1), 13-29. doi: 10.1023/a:1021171129766

Leussis M. P., & Andersen S. L. (2008). Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse, 62(1), 22-30. doi: 10.1002/syn.20462

Lonc, G. (2012). Immunolocalisation of α and β oestrogen receptors in basolateral amygdala of rabbit males. Bulletin of the Veterinary Institute in Pulawy, 56(1), 83-87. doi: 10.2478/v10213-012-0015-3

Montague, D., Weickert, C. S., Tomaskovic-Crook, E., Rothmond, D. A., Kleinman, J. E., & Rubinow, D. R. (2009). Oestrogen Receptor α Localisation in the Prefrontal Cortex of Three Mammalian Species. Journal of Neuroendocrinology, 20(7), 893-903. doi: 10.1111/j.1365-2826.2008.01743.x

Moralí, G., Larsson, K., & Beyer, C. (1977). Inhibition of testosterone-induced sexual behavior in the castrated male rat by aromatase blockers. Hormones & Behavior, 9(3), 203-213. doi: 10.1016/0018-506X(77)90056-3

Muller, M., Van Den Beld, A. W., Van Der Schouw, Y. T., Grobbe, D. E., & Lamberts, S. W. J. (2006). Effects of dehydroepiandrosterone and atamestane supplementation on frailty in elderly men. The Journal of Clinical Endocrinology & Metabolism, 91(10), 3988-3991. doi: 10.1210/jc.2005-2433

Naghdi, N., Oryan, S., & Etemadi, R. (2003). The study of spatial memory in adult male rats with injection of testosterone enanthate and flutamide into the basolateral nucleus of the amygdala in Morris water maze. Brain Research, 972(1-2), 1-8. doi: 10.1016/s0006-8993(03)02227-3

Nuñez, J. L., Huppenbauer, C. B., McAbee, M. D., Juraska, J. M., & DonCarlos, L. L. (2003). Androgen receptor expression in the developing male and female rat visual and prefrontal cortex. Journal of Neurobiology, 56(3), 293-302. doi: 10.1002/neu.10236

Paxinos, G., & Watson, C. (2007). The rat brain, in stereotaxic coordinates (6th edition). London: Elsevier.

Perelló, M., Chacon, F., Cardinali, D. P., Esquifino, A. I., & Spinedi, E. (2006). Effect of social isolation on 24-h pattern of stress hormones and leptin in rats. Life sciences, 78(16), 1857-1862. doi: 10.1016/j.lfs.2005.08.029

Poblano, A., Hernández-Godínez, B., Arellano, A., Arteaga, C., Elías, Y., Morales, J., ... Poblano-Alcalá, A. (2004). Serum testosterone and electroencephalography spectra in developmental male rhesus Macaca mulatta Monkeys. Archives of Medical Research, 35(5), 406-410. doi: 10.1016/j.arcmed.2004.06.003

Pryce, C. R. (2008). Postnatal ontogeny of expression of the corticosteroid receptor genes in mammalian brains: Inter-species and intra-species differences. Brain Research Reviews, 57(2), 596-605. doi: 10.1016/j.brainresrev.2007.08.005

Retana-Márquez, S., Bonilla-Jaime, H., Vázquez-Palacios, G., Martínez-García, R., & Velázquez-Moctezuma, J. (2003) Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Hormones & Behaviour, 44(4), 327-337. doi: 10.1016/j.yhbeh.2003.04.001

Schoenbaum, G., Chiba, A. A., & Gallagher, M. (2000). Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training. Journal of Neuroscience, 20(13), 5179-5189. doi: 10.1523/JNEUROSCI.20-13-05179.2000

Schulz, K. M., Richardson, H. N., Zehr, J. L., Osetek, A. J., Menard, T. A., & Sisk, C. L. (2004). Gonadal hormones masculinize and defeminize reproductive behaviors during puberty in the male Syriam hamster. Hormones & Behavior, 45(4), 242-249. doi: 10.1016/j.yhbeh.2003.12.007

Serra, M., Pisu, M. G., Floris, I., & Biggio, G. (2005). Social isolation-induced changes in the hypothalamic-pituitary-adrenal axis in the rat. Stress, 8(4), 259-264. doi: 10.1080/10253890500495244

Stratakis, C. A., & Chrousos, G. P. (1995). Neuroendocrinology and pathophysiology of the stress system. Annals of New York Academy of Sciences, 771(1), 1-18. doi: 10.1111/j.1749-6632.1995.tb44666.x

Vanderwolf, C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalographic and Clinical Neurophysiology, 26(4), 407-418. doi: 10.1016/0013-4694(69)90092-3

Ventura-Aquino, E., & Paredes, R. G. (2017). Animal models in sexual medicine: The need and importance of studying sexual motivation. Sexual Medicine Reviews, 5(1), 5-19. doi: 10.1016/j.sxmr.2016.07.003

Vetulani, J. (2013). Early maternal separation: A rodent model of depression and a prevailing human condition. Pharmacological Reports, 65(6), 1451-1461. doi: 10.1016/S1734-1140(13)71505-6

Wang, Y. C., Ho, U. C., Ko, M. C., Liao, C. C., & Lee, L. J. (2012). Differential neuronal changes in medial prefrontal cortex, basolateral amygdala and nucleus accumbens after postweaning social isolation. Brain Structure & Function, 217(2), 337-351. doi: 10.1007/s00429-011-0355-4

Zhang, W., & Rosenkranz, J. A. (2012). Repeated restraint stress increases basolateral amygdala neural activity in an age-dependent manner. Neuroscience, 226, 459-474. doi: 10.1016/j.neuroscience.2012.08.051