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New Research, Cognition and Behavior

Sex differences in cognitive flexibility and resting brain networks in middle-aged marmosets

M. LaClair, M. Febo, B. Nephew, N. J. Gervais, G. Poirier, K. Workman, S. Chumachenko, L. Payne, M. C. Moore, J. A. King and A. Lacreuse
eNeuro 1 July 2019, ENEURO.0154-19.2019; DOI: https://doi.org/10.1523/ENEURO.0154-19.2019
M. LaClair
1Neuroscience and Behavior Program, University of Massachusetts, Amherst, MA, 01003
2Department of Psychology, Fairfield University, Fairfield, CT, 06824
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M. Febo
3Department of Psychiatry, University of Florida, Gainsville, FL, 32610
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B. Nephew
4Worcester Polytechnic Institute, University of Massachusetts Medical School, Worcester, MA, 01655
7Center for Comparative Neuroimaging, University of Massachusetts Medical School, Worcester, MA, 01655
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N. J. Gervais
5Center for Neuroendocrine Studies, University of Massachusetts, Amherst, MA, 01003
6Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, 01003
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  • ORCID record for N. J. Gervais
G. Poirier
7Center for Comparative Neuroimaging, University of Massachusetts Medical School, Worcester, MA, 01655
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K. Workman
6Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, 01003
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S. Chumachenko
7Center for Comparative Neuroimaging, University of Massachusetts Medical School, Worcester, MA, 01655
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L. Payne
7Center for Comparative Neuroimaging, University of Massachusetts Medical School, Worcester, MA, 01655
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M. C. Moore
7Center for Comparative Neuroimaging, University of Massachusetts Medical School, Worcester, MA, 01655
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J. A. King
4Worcester Polytechnic Institute, University of Massachusetts Medical School, Worcester, MA, 01655
7Center for Comparative Neuroimaging, University of Massachusetts Medical School, Worcester, MA, 01655
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A. Lacreuse
1Neuroscience and Behavior Program, University of Massachusetts, Amherst, MA, 01003
5Center for Neuroendocrine Studies, University of Massachusetts, Amherst, MA, 01003
6Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, 01003
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ABSTRACT

Sex differences in human cognitive performance are well characterized. However, the neural correlates of these differences remain elusive. This issue may be clarified using nonhuman primates, for which sociocultural influences are minimized. We used the marmoset (Callithrix jacchus) to investigate sex differences in two aspects of executive function: Reversal Learning and Intradimensional/Extradimensional (ID/ED) set shifting. Stress reactivity and motor function were also assessed. In agreement with human literature, females needed more trials than males to acquire the reversals. No sex differences in ED set shifting or motivational measures were observed. The findings suggest enhanced habit formation in females, perhaps due to striatal estrogenic effects. Both sexes showed increased urinary cortisol during social separation stressor, but females showed an earlier increase in cortisol and a greater increase in agitated locomotion, possibly indicating enhanced stress reactivity. Independent of sex, basal cortisol predicted cognitive performance. No sex differences were found in motor performance. Associations between brain networks and reversal learning performance were investigated using resting state fMRI. Resting state functional connectivity analyses revealed sex differences in cognitive networks, with differences in overall neural network metrics and specific regions, including the prefrontal cortex, caudate, putamen, and nucleus accumbens. Correlations between cognitive flexibility and neural connectivity indicate that sex differences in cognitive flexibility are related to sex-dependent patterns of resting brain networks. Overall, our findings reveal sex differences in reversal learning, brain networks, and their relationship in the marmoset, positioning this species as an excellent model to investigate the biological basis of cognitive sex differences.

SIGNIFICANCE STATEMENT We examined sex differences in multiple outcomes (cognition, motor function, stress reactivity and resting state functional connectivity) in middle-aged marmosets. We found that female marmosets had poorer reversal learning relative to males. Resting state functional connectivity analyses revealed substantial sex differences in cognitive networks, with differences in both overall neural network metrics and specific regions, including the prefrontal cortex, caudate, putamen, and nucleus accumbens. Sex-dependent correlations between reversal learning and neural connectivity measures indicate that the sex difference in cognitive performance is related to sex-dependent patterns of resting brain networks. Although these data are correlational and cannot determine causal effects, they are consistent with human resting state data, supporting the idea that cognitive sex differences have identifiable intrinsic neural correlates.

  • Animal Models
  • Cognitive Flexibility
  • Executive Function
  • Resting State Functional Connectivity
  • Reversal Learning
  • Sex Differences;

Footnotes

  • The authors declare no conflicts of interest.

  • This study was supported by NIH grant AG 046266 to A. Lacreuse and by a dissertation fellowship from the UMass Center for Research on Families (CRF) to M. LaClair and by S10 OD018132 to J. King. Marcelo Febo acknowledges the support from the National High Magnetic Field Laboratory’s Advanced Magnetic Resonance Imaging & Spectroscopy (AMRIS) Facility (National Science Foundation Cooperative Agreement No. DMR-1157490 and the State of Florida).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Sex differences in cognitive flexibility and resting brain networks in middle-aged marmosets
M. LaClair, M. Febo, B. Nephew, N. J. Gervais, G. Poirier, K. Workman, S. Chumachenko, L. Payne, M. C. Moore, J. A. King, A. Lacreuse
eNeuro 1 July 2019, ENEURO.0154-19.2019; DOI: 10.1523/ENEURO.0154-19.2019

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Sex differences in cognitive flexibility and resting brain networks in middle-aged marmosets
M. LaClair, M. Febo, B. Nephew, N. J. Gervais, G. Poirier, K. Workman, S. Chumachenko, L. Payne, M. C. Moore, J. A. King, A. Lacreuse
eNeuro 1 July 2019, ENEURO.0154-19.2019; DOI: 10.1523/ENEURO.0154-19.2019
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Keywords

  • animal models
  • cognitive flexibility
  • Executive function
  • resting state functional connectivity
  • reversal learning
  • Sex Differences;

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