A role for puberty in water maze performance in male and female rats

Behavioral Neuroscience

Volumn 130, Issue 4, 2016, Pages 422-427

  Willing, Jari ^a   Drzewiecki, Carly M ^a   Cuenod, Bethany A ^a   Cortes, Laura R ^a   Juraska, Janice M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Adolescence; Cognitive flexibility; Prefrontal cortex; Sex differences

Indexed keywords

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; FEMALE; FUNCTIONAL ASSESSMENT; LEARNING; MALE; MEDIAL PREFRONTAL CORTEX; MENTAL DEVELOPMENT; MENTAL PERFORMANCE; MENTAL TASK; MORRIS WATER MAZE TEST; NONHUMAN; PERINATAL PERIOD; PREPUBERTY; RAT; SPATIAL MEMORY; YOUNG ADULT; ANIMAL; ANIMAL BEHAVIOR; DEPTH PERCEPTION; LONG EVANS RAT; MAZE TEST; MEMORY; PHYSIOLOGY; PREFRONTAL CORTEX; SEXUAL CHARACTERISTICS; SEXUAL MATURATION;

WATER;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; MAZE LEARNING; MEMORY; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; REVERSAL LEARNING; SEX CHARACTERISTICS; SEXUAL MATURATION; SPACE PERCEPTION; WATER;

EID: 84962659271     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/bne0000145     Document Type: Article

References (33)

1. Almey, A., Milner, T. A., & Brake, W. G. (2015). Estrogen receptors in the central nervous system and their implication for dopamine-dependent cognition in females. Hormones and Behavior, 74, 125-138. http://dx.doi.org/10.1016/j.yhbeh.2015.06.010
2. Andersen, S. L., Thompson, A. T., Rutstein, M., Hostetter, J. C., & Teicher, M. H. (2000). Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse, 37, 167-169. http://dx.doi.org/10.1002/1098-2396(200008)37:2<167::AID-SYN11>3.0.CO;2-B
3. Andrzejewski, M. E., Schochet, T. L., Feit, E. C., Harris, R., McKee, B. L., & Kelley, A. E. (2011). A comparison of adult and adolescent rat behavior in operant learning, extinction, and behavioral inhibition paradigms. Behavioral Neuroscience, 125, 93-105. http://dx.doi.org/10.1037/a0022038
4. Casey, B. J., Giedd, J. N., & Thomas, K. M. (2000). Structural and functional brain development and its relation to cognitive development. Biological Psychology, 54, 241-257. http://dx.doi.org/10.1016/S03010511(00)00058-2
5. Castellano, J. M., Bentsen, A. H., Sánchez-Garrido, M. A., Ruiz-Pino, F., Romero, M., Garcia-Galiano, D., Tena-Sempere, M. (2011). Early metabolic programming of puberty onset: Impact of changes in postnatal feeding and rearing conditions on the timing of puberty and development of the hypothalamic kisspeptin system. Endocrinology, 152, 3396-3408.
6. de Bruin, J. P., Sànchez-Santed, F., Heinsbroek, R. P., Donker, A., & Postmes, P. (1994). A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: Evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Research, 652, 323-333. http://dx.doi.org/10.1016/0006-8993(94)90243-7
7. Drzewiecki, C. M., Willing, J., & Juraska, J. M. (2015). Changes in the number of synapses in the medial prefrontal cortex across adolescence: Program No. 569.24. 2015 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2015.
8. El-Rawas, R., Saadé, N. E., Thiriet, N., Atweh, S., Jaber, M., & Al-Amin, H. A. (2009). Developmental changes in the mRNA expression of neuropeptides and dopamine and glutamate receptors in neonates and adult rats after ventral hippocampal lesion. Schizophrenia Research, 113, 298-307. http://dx.doi.org/10.1016/j.schres.2009.05.009
9. Frick, K. M., Fernandez, S. M., & Harburger, L. L. (2010). A new approach to understanding the molecular mechanisms through which estrogens affect cognition. Biochimica et Biophysica Acta, 1800, 1045-1055. http://dx.doi.org/10.1016/j.bbagen.2009.11.004
10. Gallagher, M., Burwell, R., & Burchinal, M. (2015). Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behavioral Neuroscience, 129, 540-548. http://dx.doi.org/10.1037/bne0000080
11. Juraska, J. M., & Rubinow, M. J. (2008). Hormones and memory. In H. Eichenbaum (Ed.), Learning and Memory: A Comprehensive Reference: Vol. 3. Memory systems (pp. 503-520). Oxford: Elsevier. http://dx.doi.org/10.1016/B978-012370509-9.00131-5
12. Kanit, L., Taskiran, D., Yilmaz, O. A., Balkan, B., Demirgören, S., Furedy, J. J., & Pögün, S. (2000). Sexually dimorphic cognitive style in rats emerges after puberty. Brain Research Bulletin, 52, 243-248. http://dx.doi.org/10.1016/S0361-9230(00)00232-X
13. Karatsoreos, I. N., Bhagat, S., Bloss, E. B., Morrison, J. H., & McEwen, B. S. (2011). Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. PNAS Proceedings of the National Academy of Sciences of the United States of America, 108, 1657-1662. http://dx.doi.org/10.1073/pnas.1018375108
14. Kim, J. H., & Juraska, J. M. (1997). Sex differences in the development of axon number in the splenium of the rat corpus callosum from postnatal day 15 through 60. Developmental Brain Research, 102, 77-85.
15. Korenbrot, C. C., Huhtaniemi, I. T., & Weiner, R. I. (1977). Preputial separation as an external sign of pubertal development in the male rat. Biology of Reproduction, 17, 298-303. http://dx.doi.org/10.1095/biolreprod17.2.298
16. Koss, W. A., Belden, C. E., Hristov, A. D., & Juraska, J. M. (2014). Dendritic remodeling in the adolescent medial prefrontal cortex and the basolateral amygdala of male and female rats. Synapse, 68, 61-72. http://dx.doi.org/10.1002/syn.21716
17. Koss, W. A., Franklin, A. D., & Juraska, J. M. (2011). Delayed alternation in adolescent and adult male and female rats. Developmental Psychobiology, 53, 724-731. http://dx.doi.org/10.1002/dev.20543
18. Koss, W. A., Lloyd, M. M., Sadowski, R. N., Wise, L. M., & Juraska, J. M. (2015). Gonadectomy before puberty increases the number of neurons and glia in the medial prefrontal cortex of female, but not male, rats. Developmental Psychobiology, 57, 305-312. http://dx.doi.org/10.1002/dev.21290
19. Lacroix, L., White, I., & Feldon, J. (2002). Effect of excitotoxic lesions of rat medial prefrontal cortex on spatial memory. Behavioural Brain Research, 133, 69 - 81. http://dx.doi.org/10.1016/S0166-4328(01)00442-9
20. Matsuoka, T., Sumiyoshi, T., Tsunoda, M., Takasaki, I., Tabuchi, Y., Uehara, T., Kurachi, M. (2010). Change in the expression of myelination/oligodendrocyte-related genes during puberty in the rat brain. Journal of Neural Transmission, 117, 1265-1268. http://dx.doi.org/10.1007/s00702-010-0461-0
21. Meyer, G., Ferres-Torres, R., & Mas, M. (1978). The effects of puberty and castration on hippocampal dendritic spines of mice. A Golgi study. Brain Research, 155, 108-112. http://dx.doi.org/10.1016/00068993(78)90309-8
22. Naneix, F., Marchand, A. R., Di Scala, G., Pape, J. R., & Coutureau, E. (2012). Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence. The Journal of Neuroscience, 32, 16223-16232. http://dx.doi.org/10.1523/JNEUROSCI.3080-12.2012
23. Peper, J. S., Brouwer, R. M., Schnack, H. G., van Baal, G. C., van Leeuwen, M., van den Berg, S. M., Hulshoff Pol, H. E. (2009). Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology, 34, 332-342. http://dx.doi.org/10.1016/j.psyneuen.2008.09.012
24. Rodríguez, C. A., Chamizo, V. D., & Mackintosh, N. J. (2013). Do hormonal changes that appear at the onset of puberty determine the strategies used by female rats when solving a navigation task? Hormones and Behavior, 64, 122-135. http://dx.doi.org/10.1016/j.yhbeh.2013.05.007
25. Steinberg, L. (2005). Cognitive and affective development in adolescence. Trends in Cognitive Sciences, 9, 69-74. http://dx.doi.org/10.1016/j.tics.2004.12.005
26. Sturman, D. A., Mandell, D. R., & Moghaddam, B. (2010). Adolescents exhibit behavioral differences from adults during instrumental learning and extinction. Behavioral Neuroscience, 124, 16-25. http://dx.doi.org/10.1037/a0018463
27. Tseng, K. Y., & O'Donnell, P. (2004). Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cerebral Cortex, 15, 49-57. http://dx.doi.org/10.1093/cercor/bhh107
28. Uban, K. A., Rummel, J., Floresco, S. B., & Galea, L. A. (2012). Estradiol modulates effort-based decision making in female rats. Neuropsychopharmacology, 37, 390-401. http://dx.doi.org/10.1038/npp.2011.176
29. Varlinskaya, E. I., Vetter-O'Hagen, C. S., & Spear, L. P. (2013). Puberty and gonadal hormones: Role in adolescent-typical behavioral alterations. Hormones and Behavior, 64, 343-349. http://dx.doi.org/10.1016/j.yhbeh.2012.11.012
30. Wartman, B. C., Keeley, R. J., & Holahan, M. R. (2012). Estradiol treatment in preadolescent females enhances adolescent spatial memory and differentially modulates hippocampal region-specific phosphorylated ERK labeling. Neuroscience Letters, 528, 114-119. http://dx.doi.org/10.1016/j.neulet.2012.09.018
31. Willing, J., Brodsky, J. M., Cortes, L. R., Kim, T., & Juraska, J. M. (2015). Development of dopaminergic fibers in the medial prefrontal cortex of male and female rats during adolescence: Program No. 569.12. 2015 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2015.
32. Willing, J., & Juraska, J. M. (2015). The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats. Neuroscience, 301, 268-275. http://dx.doi.org/10.1016/j.neuroscience.2015.05.073
33. Yildirim, M., Mapp, O. M., Janssen, W. G. M., Yin, W., Morrison, J. H., & Gore, A. C. (2008). Postpubertal decrease in hippocampal dendritic spines of female rats. Experimental Neurology, 210, 339-348. http://dx.doi.org/10.1016/j.expneurol.2007.11.003