Quinlan, Matthew G. and Hussain, Dema and Brake, Wayne G.
Use of Cognitive Strategies in Rats: the Role of Estradiol and its Interaction with Dopamine.
Hormones and Behavior , 53
Official URL: http://dx.doi.org/10.1016/j.yhbeh.2007.09.015
Accumulating evidence suggests a role for estrogen in the use of a particular cognitive strategy when solving a maze task. In order to confirm the role of estrogen in this phenomenon, ovariectomized (OVX) female rats receiving either high (~ 90 pg/ml) or low (~ 32 pg/ml) circulating levels of 17β-estradiol benzoate (E2) performed a plus maze task for a reward. Consistent with previous research, OVX rats receiving low levels of E2 utilized a striatum-mediated response strategy while OVX rats administered high levels of E2 employed a hippocampus-mediated place strategy. Furthermore, following a systemic injection of a moderate dose of either a dopamine D1 (SKF 83566, 0.1 mg/kg IP) or D2 (raclopride, 0.5 mg/kg IP) receptor antagonist, low E2 rats were seen to use the opposite strategy and exercise a hippocampus-mediated place strategy in order to obtain the reward. At the same doses, high E2 rats did not change from using a place strategy. At a lower dose, these drugs shifted high E2 rats such that they showed an equal propensity for either strategy; this was not observed in low E2 rats. These results corroborate previous findings that E2 plays a significant role in the use of either a response or place strategy when solving a maze for a reward. In addition, the shift in strategy after dopamine receptor blockade implies the importance of central dopamine function in selecting a cognitive strategy to solve such tasks. It is suggested that estrogen alters cognitive strategy not only by improving hippocampal function, but also by altering dopamine-regulated striatal function.
References:Becker, J. B. (1990). Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci Lett 118(2), 169-71.
Becker, J. B. (1999). Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64(4), 803-12.
Boyson, S. J., McGonigle, P., and Molinoff, P. B. (1986). Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J Neurosci 6(11), 3177-88.
Brake, W. G., Alves, S. E., Dunlop, J. C., Lee, S. J., Bulloch, K., Allen, P. B., Greengard, P., and McEwen, B. S. (2001). Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 142(3), 1284-9.
Chang, Q., and Gold, P. E. (2004). Inactivation of dorsolateral striatum impairs acquisition of response learning in cue-deficient, but not cue-available, conditions. Behav Neurosci 118(2), 383-8.
Choi, J. M., Romeo, R. D., Brake, W. G., Bethea, C. L., Rosenwaks, Z., and McEwen, B. S. (2003). Estradiol increases pre- and post-synaptic proteins in the CA1 region of the hippocampus in female rhesus macaques (Macaca mulatta). Endocrinology 144(11), 4734-8.
Compton, D. M. (2004). Behavior strategy learning in rat: effects of lesions of the dorsal striatum or dorsal hippocampus. Behav Processes 67(3), 335-42.
Cook, D., and Kesner, R. P. (1988). Caudate nucleus and memory for egocentric localization. Behav Neural Biol 49(3), 332-43.
Cordoba Montoya, D. A., and Carrer, H. F. (1997). Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res 778(2), 430-8.
Daniel, J. M., and Lee, C. D. (2004). Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze. Neurobiol Learn Mem 82(2), 142-9.
Daniel, J. M., Sulzer, J. K., and Hulst, J. L. (2006). Estrogen increases the sensitivity of ovariectomized rats to the disruptive effects produced by antagonism of D2 but not D1 dopamine receptors during performance of a response learning task. Horm Behav 49(1), 38-44.
Davis, D. M., Jacobson, T. K., Aliakbari, S., and Mizumori, S. J. (2005). Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiol Learn Mem 84(2), 132-7.
Day, M., and Good, M. (2005). Ovariectomy-induced disruption of long-term synaptic depression in the hippocampal CA1 region in vivo is attenuated with chronic estrogen replacement. Neurobiol Learn Mem 83(1), 13-21.
Di Paolo, T., Poyet, P., and Labrie, F. (1981). Effect of chronic estradiol and haloperidol treatment on striatal dopamine receptors. Eur J Pharmacol 73(1), 105-6.
Domenger, D., and Schwarting, R. K. (2006). The serial reaction time task in the rat: effects of D1 and D2 dopamine-receptor antagonists. Behav Brain Res 175(2), 212-22.
Graybiel, A. M. (2005). The basal ganglia: learning new tricks and loving it. Curr Opin Neurobiol 15(6), 638-44.
Hampson, E. (1995). Spatial cognition in humans: possible modulation by androgens and estrogens. J Psychiatry Neurosci 20(5), 397-404.
Holmes, M. M., Wide, J. K., and Galea, L. A. (2002). Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav Neurosci 116(5), 928-34.
Hu, M., Watson, C. J., Kennedy, R. T., and Becker, J. B. (2006). Estradiol attenuates the K+-induced increase in extracellular GABA in rat striatum. Synapse 59(2), 122-4.
Jovanovic, T., Szilagyi, S., Chakravorty, S., Fiallos, A. M., Lewison, B. J., Parwani, A., Schwartz, M. P., Gonzenbach, S., Rotrosen, J. P., and Duncan, E. J. (2004). Menstrual cycle phase effects on prepulse inhibition of acoustic startle. Psychophysiology 41(3), 401-6.
Kesner, R. P. (1990). Memory for frequency in rats: role of the hippocampus and medial prefrontal cortex. Behav Neural Biol 53(3), 402-10.
Koch, M. (1998). Sensorimotor gating changes across the estrous cycle in female rats. Physiol Behav 64(5), 625-8.
Korol, D. L., and Kolo, L. L. (2002). Estrogen-induced changes in place and response learning in young adult female rats. Behav Neurosci 116(3), 411-20.
Korol, D. L., Malin, E. L., Borden, K. A., Busby, R. A., and Couper-Leo, J. (2004). Shifts in preferred learning strategy across the estrous cycle in female rats. Horm Behav 45(5), 330-8.
Levesque, D., and Di Paolo, T. (1989). Chronic estradiol treatment increases ovariectomized rat striatal D-1 dopamine receptors. Life Sci 45(19), 1813-20.
Lubow, R. E. (1997). Latent inhibition as a measure of learned inattention: some problems and solutions. Behav Brain Res 88(1), 75-83.
Mannino, C. A., South, S. M., Inturrisi, C. E., and Quinones-Jenab, V. (2005). Pharmacokinetics and effects of 17beta-estradiol and progesterone implants in ovariectomized rats. J Pain 6(12), 809-16.
Matthews, D. B., Simson, P. E., and Best, P. J. (1995). Acute ethanol impairs spatial memory but not stimulus/response memory in the rat. Alcohol Clin Exp Res 19(4), 902-9.
McDonald, R. J., and White, N. M. (1994). Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 61(3), 260-70.
McEwen, B., Akama, K., Alves, S., Brake, W. G., Bulloch, K., Lee, S., Li, C., Yuen, G., and Milner, T. A. (2001). Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci U S A 98(13), 7093-100.
McIntyre, C. K., Marriott, L. K., and Gold, P. E. (2003). Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol Learn Mem 79(2), 177-83.
Mizumori, S. J., Yeshenko, O., Gill, K. M., and Davis, D. M. (2004). Parallel processing across neural systems: implications for a multiple memory system hypothesis. Neurobiol Learn Mem 82(3), 278-98.
Nofrey, B. S., Ben-Shahar, O. M., and Brake, W. G. (2007). Estrogen abolishes latent inhibition in ovariectomized female rats. Brain Cogn in press.
Packard, M. G., and McGaugh, J. L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65(1), 65-72.
Quinlan, M. G., Graffe, N., Duncan, A., and Brake, W. G. (2006). Postpubertal but not prepubertal rats show sex differences in latent inhibition, Society for Neuroscience Abstracts.
Salamone, J. D., Arizzi, M. N., Sandoval, M. D., Cervone, K. M., and Aberman, J. E. (2002). Dopamine antagonists alter response allocation but do not suppress appetite for food in rats: contrast between the effects of SKF 83566, raclopride, and fenfluramine on a concurrent choice task. Psychopharmacology (Berl) 160(4), 371-80.
Serafim, A. P., and Felicio, L. F. (2001). Dopaminergic modulation of grooming behavior in virgin and pregnant rats. Braz J Med Biol Res 34(11), 1465-70.
Shaham, Y., and Stewart, J. (1996). Effects of opioid and dopamine receptor antagonists on relapse induced by stress and re-exposure to heroin in rats. Psychopharmacology (Berl) 125(4), 385-91.
Sherwin, B. B. (2003). Estrogen and cognitive functioning in women. Endocr Rev 24(2), 133-51.
Warren, S. G., Humphreys, A. G., Juraska, J. M., and Greenough, W. T. (1995). LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res 703(1-2), 26-30.
White, N. M., and McDonald, R. J. (2002). Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 77(2), 125-84.
Wide, J. K., Hanratty, K., Ting, J., and Galea, L. A. (2004). High level estradiol impairs and low level estradiol facilitates non-spatial working memory. Behav Brain Res 155(1), 45-53.
Williams, C. L., Barnett, A. M., and Meck, W. H. (1990). Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104(1), 84-97.
Wise, R. A., and Carlezon, W. A., Jr. (1994). Attenuation of the locomotor-sensitizing effects of the D2 dopamine agonist bromocriptine by either the D1 antagonist SCH 23390 or the D2 antagonist raclopride. Synapse 17(3), 155-9.
Woolley, C. S., and McEwen, B. S. (1992). Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci 12(7), 2549-54.
Zurkovsky, L., Brown, S. L., Boyd, S. E., Fell, J. A., and Korol, D. L. (2007). Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience 144(1), 26-37.
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