Animal Cognition

, Volume 19, Issue 3, pp 619–630 | Cite as

Reversal learning in gonadectomized marmosets with and without hormone replacement: are males more sensitive to punishment?

  • Matthew LaClair
  • Agnès LacreuseEmail author
Original Paper


This study examined sex differences in executive function in middle-aged gonadectomized marmosets (Callithrix jacchus) with or without hormonal replacement. We tested ten castrated male (mean age 5.5 years) marmosets treated with testosterone cypionate (T, n = 5) or vehicle (n = 5) on Reversal Learning, which contributes to cognitive flexibility, and the Delayed Response task, measuring working memory. Their performance was compared to that of 11 ovariectomized females (mean age = 3.7 years) treated with Silastic capsules filled with 17-β estradiol (E2, n = 6) or empty capsules (n = 5), previously tested on the same tasks (Lacreuse et al. in J Neuroendocrinol 26:296–309, 2014. doi: 10.1111/jne.12147). Behavioral observations were conducted daily. Females exhibited more locomotor behaviors than males. Males and females did not differ in the number of trials taken to reach criterion on the reversals, but males had significantly longer response latencies, regardless of hormone replacement. They also had a greater number of refusals than females. Additionally, both control and T-treated males, but not females, had slower responses on incorrect trials, suggesting that males were making errors due to distraction, lack of motivation or uncertainty. Furthermore, although both males and females had slower responding following an incorrect compared to a correct trial, the sex difference in response latencies was disproportionally large following an incorrect trial. No sex difference was found in the Delayed Response task. Overall, slower response latencies in males than females during Reversal Learning, especially during and following an incorrect trial, may reflect greater sensitivity to punishment (omission of reward) and greater performance monitoring in males, compared to females. Because these differences occurred in gonadectomized animals and regardless of hormone replacement, they may be organized early in life.


Cognitive flexibility Estrogen Executive function Response inhibition Testosterone Working memory 



This research was supported in part by NIH grant # MH091492 to Agnès Lacreuse and a graduate student grant from the UMass Center for Research on Families (CRF) to Matthew LaClair. We are very grateful to Jeemin Chang for his assistance with many aspects of this project. We also thank Karen Bui, Raymond Guigni, Alexander McFarland, Jocelyn Mejia, Molly Morgan, Katharine Newman, Christine O’Brien and Courtney Tolliday for their help with data collection. We thank the UMass Veterinary Staff, Animal Care Staff and Shop staff for their expert assistance. We also thank the CRF for statistical consult.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.


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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Neuroscience and Behavior ProgramUniversity of MassachusettsAmherstUSA
  2. 2.Department of Psychological and Brain SciencesUniversity of MassachusettsAmherstUSA

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