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Differential Effect of Acute Stress on Visuospatial Working Memory and Sexual Motivation in Male Rats

DOI: 10.4236/jbbs.2015.57023   PDF   HTML   XML   3,474 Downloads   3,953 Views   Citations

Abstract

Working memory is an executive function that is highly dependent on the functioning of the prefrontal cortex. Several studies using food or drink as rewards have demonstrated that rats are capable of performing tasks that involve working memory. Sexual behavior is another highly-rewarding, motivated behavior that has proven to be an efficient incentive in classical operant tasks. Considering that both sexual behavior and working memory are sensitive to the effects of stress, the aim of this study was to determine the effect of acute stress on visuospatial working memory during a sexually-motivated task (a nonmatching-to-sample task in a T-maze) in male rats. Thirty-two male Wistar rats were trained in the T-maze using sexual interaction (intromission and ejaculation) as a reinforcer during a 4-day training period (training sessions held every 4th day). On the basis of their performance, the rats were classified as good-learners (n = 12) and bad-learners (n = 20), and on the fifth day, 6 good-learners and 10 bad-learners were subjected to stress using the cold water immersion model (CWI, 15°C) for 15 minutes before they were evaluated in the T-maze. The remaining rats made up the control group (i.e., they performed the task without previous stress). Results showed that acute stress by CWI improved working memory in the bad-learners but did not affect the performance of the good-learners, although in both groups (good- and bad-learners) stress decreased the sexual motivation to perform the task. It is probable that the increased levels of corticosterone in the stress situation could activate glutamatergic transmission in the prefrontal cortex, thus facilitating working memory and, simultaneously, decreasing testosterone levels, which exerts a negative effect on sexual motivation in these male rats.

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Hernández-González, M. , Hernández-Arteaga, E. , Almanza-Sepúlveda, M. and Guevara, M. (2015) Differential Effect of Acute Stress on Visuospatial Working Memory and Sexual Motivation in Male Rats. Journal of Behavioral and Brain Science, 5, 221-230. doi: 10.4236/jbbs.2015.57023.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Stratakis, C.A. and Chrousos, G.P. (1995) Neuroendocrinology and Pathophysiology of the Stress System. Annals of the New York Academy of Sciences, 771, 1-18.
http://dx.doi.org/10.1111/j.1749-6632.1995.tb44666.x
[2] Dhabhar, F.S., Malarkey, W.B., Neri E. and McEwen, B.S. (2012) Stress-Induced Redistribution of Immune Cells from Barracks to Boulevards to Battlefields: A Tale of Three Hormones—Curt Richter Award Winner. Psychoneuroendocrinology, 37, 1345-1368.
http://dx.doi.org/10.1016/j.psyneuen.2012.05.008
[3] Tafet, G.E. and Bernardini, R. (2003) Psychoneuroendocrinological Links between Chronic Stress and Depression. Progress in Neuro-Psychopharmacology Biological Psychiatry, 27, 893-903.
http://dx.doi.org/10.1016/S0278-5846(03)00162-3
[4] Butts, K.A., Ewinberg, J., Young, A.H. and Phillips, A.G. (2011) Glucocorticoid Receptors in the Prefrontal Cortex Regulate Stress-Evoked Dopamine Efflux and Aspects of Executive Function. PNAS, 18, 459-464.
http://dx.doi.org/10.1073/pnas.1111746108
[5] Murphy, B.L., Arsten, A.F.T., Goldman-Rakic, P.S. and Roth, R.H. (1996) Incresead Dopamine Turnover in the Prefrontal Cortex Impairs Spatial Working Memory Performance in Rats and Monkeys. PNAS, 93, 1325-1329.
http://www.pnas.org/content/93/3/1325.full.pdf
http://dx.doi.org/10.1073/pnas.93.3.1325
[6] Devilbiss, D.M., Jenison, R.L. and Berridge, C.W. (2012) Stress-Induce Impairment of a Working Memory Task: Role of Spiking Rate and Spiking History Predicted Discharge. PLOS Computational Biology, 8, 1-14.
http://dx.doi.org/10.1371/journal.pcbi.1002681
[7] Sandi, C., Loscertales, M. and Guaza, C. (1997) Experience-Dependent Facilitating Effect of Corticosterone on Spatial Memory Formation in the Water Maze. European Journal of Neuroscience, 9, 637-642.
http://dx.doi.org/10.1111/j.1460-9568.1997.tb01412.x
[8] Yuen, E.Y., Liu, W., Karatsoreos, I.N., Feng, J., McEwen, B.S. and Yan, Z. (2009) Acute Stress Enhances Glutamatergic Transmission in Prefrontal Cortex and Facilitates Working Memory. PNAS, 106, 14075-14079.
http://dx.doi.org/10.1073/pnas.0906791106
[9] Yuen, E.Y., Liu, W., Karatsoreos, I.N., Ren, Y., Feng, J., McEwen, B.S. and Yan, Z. (2011) Mechanisms for Acute Stress-Induced Enhancement of Glutamatergic Transmission and Working Memory. Molecular Psychiatry, 16, 156-170.
http://dx.doi.org/10.1038/mp.2010.50
[10] Goldman-Rakic, P.S. (1996) Regional and Cellular Fractionation of Working Memory. PNAS, 93, 13473-13480.
http://www.pnas.org/content/93/24/13473.full.pdf
http://dx.doi.org/10.1073/pnas.93.24.13473
[11] Petrides, M. (2005) Lateral Prefrontal Cortex: Architectonic and Functional Organization. Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 781-795.
http://dx.doi.org/10.1098/rstb.2005.1631
[12] Gisquet-Verrier, P. and Delatour, B. (2006) The Role of the Rat Prelimbic/Infralimbic Cortex in Working Memory: Not Involved in the Short-Term Maintenance but in Monitoring and Processing Functions. Neuroscience, 141, 585-596.
http://dx.doi.org/10.1016/j.neuroscience.2006.04.009
[13] Kagan, J. (1955) Differential Reward Value of Incomplete and Complete Sexual Behavior. Journal of Comparative and Physiological Psychology, 48, 59-64.
http://dx.doi.org/10.1037/h0043461
[14] Whalen, R.E. (1961) Effects of Mounting without Intromission and Intromission without Ejaculation on Sexual Behavior and Maze Learning. Journal of Comparative and Physiological Psychology, 54, 409-415.
http://dx.doi.org/10.1037/h0046385
[15] Agmo, A. (1999) Sexual Motivation—An Inquiry into Events Determining the Occurrence of Sexual Behavior. Behavioural Brain Research, 105, 129-150.
http://dx.doi.org/10.1016/S0166-4328(99)00088-1
[16] Hernández-González, M., Prieto-Beracoechea, C.A., Arteaga-Silva, M. and Guevara, M.A. (2007) Different Functionality of the Medial and Orbital Prefrontal Cortex during a Sexually Motivated Task in Rats. Physiology & Behavior, 90, 450-458.
http://dx.doi.org/10.1016/j.physbeh.2006.10.006
[17] Tenk, C.M., Wilson, H., Zhang, Q., Pitchers, K.K. and Coolen, L.M. (2009) Sexual Reward in Male Rats: Effects of Sexual Experience on Conditioned Place Preferences Associated with Ejaculation and Intromissions. Hormones and Behavior, 55, 93-97.
http://dx.doi.org/10.1016/j.yhbeh.2008.08.012
[18] Hernández-González, M., Almanza-Sepúlveda, M.L., Olvera-Cortés, M.E., Gutiérrez-Guzmán, B.E. and Guevara, M.A. (2012) Prefrontal Electroencephalographic Activity during the Working Memory Processes Involved in a Sexually Motivated Task in Male Rats. Experimental Brain Research, 221, 143-153.
http://dx.doi.org/10.1007/s00221-012-3155-z
[19] Beach, F.A. and Jordan, L. (1956) Effects of Sexual Reinforcement upon the Performance of Male Rats in a Straight Runway. Journal of Comparative and Physiological Psychology, 49, 105-111.
http://dx.doi.org/10.1037/h0046471
[20] Almanza Sepúlveda, M.A., Gutiérrez Guzmán, B.E., Olvera Cortés, M.E., Guevara, M.A. and Hernández-González, M. (2010) Modelo de memoria de trabajo en ratas macho sexualmente motivadas. Scientia-CUCBA, 12, 39-49.
[21] Retana-Márquez, S., Bonilla-Jaime, H., Vázquez-Palacios, G., Martínez-García, R. and Velázquez-Moctezuma, J. (2003) Changes in Masculine Sexual Behavior, Corticosterone and Testosterone in Response to Acute and Chronic Stress in Male Rats. Hormones and Behavior, 44, 327-337.
http://dx.doi.org/10.1016/j.yhbeh.2003.04.001
[22] Larsson, K. (1963) Non-Specific Stimulation and Sexual Behavior in the Male Rat. Behavior, 20, 110-114.
http://dx.doi.org/10.1163/156853963X00239
[23] Barfield, R. and Sachs, B. (1968) Sexual Behavior Stimulation by Painful Electrical Shock to Skin in Male Rats. Science, 161, 192-395.
http://dx.doi.org/10.1126/science.161.3839.392
[24] Menéndez-Patterson, A., Flores-Lozano, J.A., Fernández, S. and Marín, B. (1978) Stress and Sexual Behavior in Male Rats. Physiology & Behavior, 24, 403-406.
http://dx.doi.org/10.1016/0031-9384(80)90106-7
[25] Retana-Márquez, S., Domínguez-Salazar, E. and Velázquez-Moctezuma, J. (1996) Effect of Acute and Chronic Stress on Masculine Sexual Behavior in the Rat. Psychoneuroendocrinology, 21, 39-50.
http://dx.doi.org/10.1016/0306-4530(95)00029-1
[26] Rocher, C., Spedding, M., Munoz, C. and Jay, T.M. (2004) Acute Stress-Induced Changes in Hippocampal/Prefrontal Circuits in Rats: Effects of Antidepressants. Cerebral Cortex, 14, 224-229.
http://dx.doi.org/10.1093/cercor/bhg122
[27] Diamond, D.M., Fleshner, M., Ingersoll, N. and Rose, G.M. (1996) Psychological Stress Impairs Spatial Working Memory: Relevance to Electrophysiological Studies of Hippocampal Function. Behavioral Neuroscience, 110, 661-672.
http://dx.doi.org/10.1037/0735-7044.110.4.661
[28] McEwen, B.S. and Chattarji, S. (2004) Molecular Mechanisms of Neuroplasticity and Pharmacological Implications: The Example of Tianeptine. European Neuropsy-chopharmacology, 14, 497-502.
http://dx.doi.org/10.1016/j.euroneuro.2004.09.008
[29] Frajese, G., Lazzari, R., Magnani, A., Moretti, C., Sforza, V. and Nerozzi, D. (1990) Neurotransmitter, Opiodergic System, Steroid-Hormone Interaction and Involvement in the Replacement Therapy of Sexual Disorders. The Journal of Steroid Biochemistry and Molecular Biology, 37, 411-419.
http://dx.doi.org/10.1016/0960-0760(90)90492-4
[30] Guevara, M.A., Amezcua, C.C., Hernández-González, M. and Sanz, A. (2012) Sexy Mater: programa computacional para el registro y análisis de conductas sexuales y maternales en roedores. Neurobiología, Revista Electrónica, 12, 1-13.
[31] Sánchez-Santed, F., de Bruin, J.C.P., Heinsbroek, R.P.W. and Verwer, R.W.H. (1997) Spatial Delayed Alteration of Rats in a T-Maze: Effects of Neurotoxic Lesions of the Medial Prefrontal Cortex and of T-Maze Rotations. Behavioural Brain Research, 84, 73-79.
http://dx.doi.org/10.1016/S0166-4328(97)83327-X
[32] Arnsten, A.F.T. and Goldman-Rakic, P.S. (1998) Noise Stress Impairs Prefrontal Cortical Cognitive Function in Monkeys. Archives of General Psychiatry, 55, 362-368.
http://dx.doi.org/10.1001/archpsyc.55.4.362
[33] Quervain, D.J.F., Aerni, A., Schelling, G. and Roozendaal, B. (2009) Glucocorticoids and the Regulation of Memory in Health and Disease. Frontiers in Neuroendocrinology, 30, 358-370.
http://dx.doi.org/10.1016/j.yfrne.2009.03.002
[34] Roozendaal, B., McReynolds, J.R. and McGaugh, J.L. (2004) The Basolateral Amygdala Interacts with the Medial Prefrontal Cortex in Regulating Glucocorticoid Effects on Working Memory Impairment. Journal of Neuroscience, 24, 1385-1392.
http://dx.doi.org/10.1523/JNEUROSCI.4664-03.2004
[35] Mani, S.K., Allen, J.M., Clark, J.H., Blaustein, J.D. and O’Malley, B.W. (1994) Convergent Pathways for Steroid Hormone- and Neurotransmitter-Induced Rat Sexual Behavior. Science, 265, 1246-1249.
http://dx.doi.org/10.1126/science.7915049
[36] Paredes, R.G. (2009) Evaluating the Neurobiology of Sexual Reward. ILAR Journal, 50, 15-27.
http://dx.doi.org/10.1093/ilar.50.1.15
[37] Coddington, E., Lewis, C., Rose, J.D. and Moore, F.L. (2007) Endocannabinoids Mediate the Effects of Acute Stress and Corticosterone on Sex Behavior. Endocrinology, 148, 493-500.
http://dx.doi.org/10.1210/en.2006-0740
[38] Dickens, M.J., Cornil, C.A. and Balthazart, J. (2011) Acute Stress Differentially Affects Aromatase Activity in Specific Brain Nuclei of Adult Male and Female Quail. Endocrinology, 152, 4242-4251.
http://dx.doi.org/10.1210/en.2011-1341
[39] Rodríguez-Manzo, G., López-Rubalcava, C. and Fernández-Guasti, A. (1999) Anxiolytic-Like Effect of Ejaculation under Various Sexual Behavior Conditions in the Male Rat. Physiology & Behavior, 67, 651-657.
http://dx.doi.org/10.1016/S0031-9384(99)00119-5
[40] Fernández-Guasti, A., Roldán-Roldán, G. and Saldívar, A. (1989) Reduction in Anxiety after Ejaculation in the Rat. Behavioural Brain Research, 32, 23-29.
http://dx.doi.org/10.1016/S0166-4328(89)80068-3

  
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