Testicular hormones mediate robust sex differences in impulsive choice in rats

  1. Caesar M Hernandez
  2. Caitlin Orsini
  3. Alexa-Rae Wheeler
  4. Tyler W Ten Eyck
  5. Sara M Betzhold
  6. Chase C Labiste
  7. Noelle G Wright
  8. Barry Setlow
  9. Jennifer L Bizon  Is a corresponding author
  1. Department of Neuroscience, University of Florida, United States
  2. Department of Psychiatry, University of Florida, United States
7 figures and 1 additional file

Figures

Intertemporal choice task and experiment timeline.

(A) Timeline of experiments. (B) Schematic of the intertemporal choice task illustrating the choices and trial blocks across which the duration of the delay to the large reward increased. On each trial, rats were presented with two response levers that differed with respect to the magnitude and timing of associated reward delivery. A press on one lever delivered a small (one food pellet), immediate reward, whereas a press on the other lever delivered a large (four food pellets), delayed reward. Trials were presented in a blocked design, such that the delay to the large reward increased across successive blocks of trials in a session.

Effect of sex on impulsive choice.

(A) Mean percent choice of the large reward in male and female rats. Female rats showed greater impulsive choice relative to males. (B) Impulsive choice in females did not fluctuate across the estrous cycle. In all panels, error bars represent the standard error of the mean (SEM). **p<0.01, main effect of sex; ××××p < 0.001, sex × delay interaction; +p<0.05, ++p<0.01, +++p<0.001, post-hoc t-tests sex difference at each delay. Raw data for these graphs are provided in Figure 2—source data 1 and 2.

Effect of sex on forced-choice lever response latency and omissions.

(A) As delays to large reward delivery increased, latency to press the large reward lever during forced-choice trials also increased in both sexes; however, this effect was more robust in females such that there was a main effect of lever in females but not in males. (B) While forced-choice trial omissions did not increase in males as a function of delay, females omitted significantly more forced-choice trials corresponding to the large reward lever at longer delays. In all panels, error bars represent standard error of the mean (SEM). ****p<0.001, main effect of lever; ××××p < 0.001, lever × delay interaction. +p<0.05, ++p<0.01, +++p<0.001, post-hoc t-tests lever latency/omission difference at each delay. Raw data for these graphs are provided in Figure 3—source data 1 and 2.

Figure 3—source data 1

Figure 3A Sex difference in forced choice lever response latencies.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig3-data1-v1.xlsx
Figure 3—source data 2

Figure 3B Sex difference in forced choice trial omissions.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig3-data2-v1.xlsx
Effect of ad libitum feeding schedule on choice performance.

(A) Relative to a food restriction feeding schedule, ad libitum feeding for 1 hr prior to testing shifted rats’ preference towards small, immediate rewards, but did not differentially affect choice performance in males and females. (B) There was a main effect of ad libitum feeding relative to food-restricted feeding, averaged across all delays shown in A. Each rat’s percentage choice of the large reward averaged across all delays is represented by an individual data point. (C) As expected, 1 hr of ad libitum feeding prior to testing increased free-choice trial omissions in all rats. (D-F) Similar methodology and data presentation as A-C except that data were collected after ad libitum feeding for 24 hr prior to testing. As with the 1 hr ad libitum schedule, the 24 hr ad libitum feeding did not differentially affect choice performance in males and females. In all panels, error bars represent standard error of the mean (SEM). *p<0.05, **p<0.01, ***p<0.001. Raw data for these graphs are provided in Figure 4—source data 16.

Figure 4—source data 1

Figure 4A Effect of 1-hour ad libitum feeding on intertemporal choice.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig4-data1-v1.xlsx
Figure 4—source data 2

Figure 4B Effect of 1-hour ad libitum feeding on intertemporal choice (collapsed across delays).

https://cdn.elifesciences.org/articles/58604/elife-58604-fig4-data2-v1.xlsx
Figure 4—source data 3

Figure 4C Effect of 1-hour ad libitum feeding on free-choice trial omissions.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig4-data3-v1.xlsx
Figure 4—source data 4

Figure 4D Effect of 24-hour ad libitum feeding on intertemporal choice.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig4-data4-v1.xlsx
Figure 4—source data 5

Figure 4E Effect of 24-hour ad libitum feeding on intertemporal choice (collapsed across delays).

https://cdn.elifesciences.org/articles/58604/elife-58604-fig4-data5-v1.xlsx
Figure 4—source data 6

Figure 4F Effect of 24-hour ad libitum feeding on free-choice trial omissions.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig4-data6-v1.xlsx
Effect of ovariectomy (OVX) on choice performance in female rats.

(A) There were no significant changes in choice performance in either OVX or sham females after surgery. (B) Free-choice trial omissions in sham and ovariectomized female groups prior to and post surgeries. OVX had no effect on free-choice trial omissions. (C) Adjusting the intertemporal choice task to incorporate shorter delays did not reveal an effect of OVX. In all panels, error bars represent standard error of the mean (SEM). Raw data for these graphs are provided in Figure 5—source data 13.

Figure 5—source data 1

Figure 5A Effect of ovariectomy on intertemporal choice.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig5-data1-v1.xlsx
Figure 5—source data 2

Figure 5B Effect of ovariectomy on free-choice trial omissions.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig5-data2-v1.xlsx
Figure 5—source data 3

Figure 5C Effect of ovariectomy on intertemporal choice (shorter delays).

https://cdn.elifesciences.org/articles/58604/elife-58604-fig5-data3-v1.xlsx
Effect of orchiectomy (ORX) on choice performance in male rats.

(A) Choice performance in shams was unchanged post-surgery relative to pre-surgery; however, ORX caused an increase in impulsive choice post-surgery relative to pre-surgery. (B) Main effect of surgery in both sham and orchiectomized rats. Each rat’s percent choice of the large reward (averaged across all delays) is represented by an individual data point. (C) Free-choice trial omissions in sham and orchiectomized male groups prior to and post surgeries. ORX had no effect on free-choice trial omissions. In all panels, error bars represent standard error of the mean (SEM). ×p<0.05, group × phase × delay interaction. #p<0.07, post-hoc t-tests group difference at each delay. Raw data for these graphs are provided in Figure 6—source data 13.

Figure 6—source data 1

Figure 6A Effect of orchiectomy on intertemporal choice.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig6-data1-v1.xlsx
Figure 6—source data 2

Figure 6B Effect of orchiectomy on intertemporal choice (collapsed across delays).

https://cdn.elifesciences.org/articles/58604/elife-58604-fig6-data2-v1.xlsx
Figure 6—source data 3

Figure 6C Effect of orchiectomy on free-choice trial omissions.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig6-data3-v1.xlsx
Effect of orchiectomies on forced-choice lever response latency and omissions.

(A) As delays to large reward delivery increased, large reward lever response latency during forced-choice trials also increased in males in the orchiectomy group; however, the effect was more robust after orchiectomy, such that there was a main effect of lever that was absent pre-surgery. (B) While forced-choice trial omissions did not increase at longer delays prior to surgery in orchiectomized rats, after surgery, the rats numerically (though not significantly) omitted more large reward forced-choice trials at longer delays. In all panels, error bars represent standard error of the mean (SEM). *p<0.05, main effect of lever; ××××p < 0.001, lever × delay block interaction. #p<0.07, +p<0.05, +++p<0.001, post-hoc t-tests lever latency difference at each delay. Raw data for these graphs are provided in Figure 7—source data 1 and 2.

Figure 7—source data 1

Figure 7A Effect of orchiectomy on forced choice lever response latencies.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig7-data1-v1.xlsx
Figure 7—source data 2

Figure 7B Effect of orchiectomy on forced choice trial omissions.

https://cdn.elifesciences.org/articles/58604/elife-58604-fig7-data2-v1.xlsx

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  1. Caesar M Hernandez
  2. Caitlin Orsini
  3. Alexa-Rae Wheeler
  4. Tyler W Ten Eyck
  5. Sara M Betzhold
  6. Chase C Labiste
  7. Noelle G Wright
  8. Barry Setlow
  9. Jennifer L Bizon
(2020)
Testicular hormones mediate robust sex differences in impulsive choice in rats
eLife 9:e58604.
https://doi.org/10.7554/eLife.58604