Gender Differences in Reward-Related Decision Processing
Gender Differences in Reward-Related Decision Processing
The cold pressor nearly doubled mean cortisol levels in stress subjects, while cortisol levels did not change in controls, F1,43 = 25.56, P = 0.000002 (Figure 2). Although mean cortisol levels were higher in males, overall, F1,43 = 5.15, P = 0.03, there were no main effects of gender on cortisol change, F1,43 < 1, nor was there a gender-by-stress condition interaction, F1,43 < 1. The effect of the stressor on cortisol elevation remained highly significant after excluding participants from the analysis who did not complete the full 3-min cold pressor challenge (see Results in Supplementary Data). These results indicate that the cold pressor reliably elevated cortisol levels without significant gender-specific effects.
(Enlarge Image)
Figure 2.
Cortisol levels increased significantly in the stress group (cold pressor) but not in the control group (warm water). Cortisol responses to stress were not dependent on gender. Poststress cortisol is the average of cortisol at 21 and 35 min after the start of the hand immersion task (s2, s3, respectively); immediately before and just after the decision task. Error bars represent s.e.m.
Postexperiment ratings of stress resulting from the hand immersion task indicated that subjective stress experienced by participants in the cold pressor group was greater than that experienced by the control group, F1,43 = 231.75, P < 0.000001 (Mstress = 5.11 ± 1.41; Mcontrol = 1.04 ± 0.21). Subjective responses to the cold pressor were greater in women than in men, F1,43 = 4.57, P = 0.04 (Mwomen = 5.73 ± 0.91; Mmen = 4.50 ± 1.57), with no gender differences in the control group (Mwomen = 1.0 ± 0.00; Mmen = 1.08 ± 0.29), resulting in a gender-by-stress interaction, F1,43 = 6.00, P = 0.02. Additional analyses indicated that gender differences in stress-modulated decision processing were not simply the result of greater subjective stress response in females compared with males (see Results in Supplementary Data).
Consistent with our previous behavioral findings (Lighthall et al., 2009), BART behavior and earnings were similar for males and females under control conditions, but diverged with stress, leading to a gender-by-stress interaction. As displayed in Figure 3, stress increased gender differences in reward collection rate (mean number of balloons 'cashed out'), F1,43 = 4.82, P = 0.03, decision speed (button pressing intervals), F1,43 = 4.79, P = 0.03 and total earnings, F1,43 = 7.93, P = 0.007. Examination of confidence intervals indicated no gender differences in these outcome measures in the control condition, only in the stress condition. While gender-by-stress interactions were observed for these measures, individual cortisol change values were not correlated with any of the behavioral outcomes across conditions or within any groups (P's > 0.05). Regarding our measure of risk taking (mean number of pumps per balloon for nonexploding balloons), we did not find any differences by stress condition, F1,43 < 1, gender, F1,43 < 1, nor was there a gender-by-stress interaction, F1,43 < 1. Relative to the number of pumps possible per balloon (maximum = 90), the average number of pumps was fairly low across groups (M = 19.39 ± 2.38), indicating low risk taking overall. As the likelihood of losses ('explosions') during the BART increased with the number of pumps per balloon, the average number of explosions experienced per block was also low across conditions (M = 2.59 ± 0.31). There were no significant group differences or interactions in the number of explosions per block (P's > 0.05); as may be expected given the low number of pumps per balloon on average.
(Enlarge Image)
Figure 3.
Gender-by-stress effects on behavior and earnings in the BART. Group means for number of balloons completed per active block (A), decision speed (B) and total earnings in US dollars across all four active blocks (C). Error bars represent s.e.m.
While risk taking was not modulated by gender or stress in this study, our fMRI-adapted BART differed from the original task (Lejuez et al., 2002) in that the number of balloons played was only limited by the duration of active blocks. This introduced a potentially successful strategy—not present in the original BART—of playing as many balloons as quickly as possible in order to earn more money. Notably, Pearson's correlations confirmed that balloon count and decision speed were related to earnings (R47 = 0.33, P = 0.03; R47 = −0.76, P < 0.000001, respectively). Direction of stress effects by gender indicated that, from an earnings standpoint, stress led to more profitable decision behavior in males but less profitable behavior in females
See Supplementary Data in the Results section for 'Subjective stress: Scan session and BART effort'.
As expected, decision-related activation (active–passive contrast) across groups was observed in regions associated with motivation and decision making. In particular, the decision task resulted in robust activation of the thalamus, putamen, caudate, anterior cingulate, dorsolateral and ventrolateral PFC, insula, inferior parietal lobe and inferior frontal gyrus. Significant clusters were also apparent in sensorimotor and visual structures (Supplementary Table S1). Further details on passive task-related activation and group differences by gender and stress can be found in Results in Supplementary Data. Of primary interest, group level analysis of decision-related activation revealed gender-by-stress interactions in motivation and decision regions; most notably in the left dorsal striatum (putamen) and left anterior insula (Figure 4 and Table 1). Gender–stress interactions were also apparent in sensorimotor and visual regions.
(Enlarge Image)
Figure 4.
Whole-brain analysis revealed significant gender–stress interactions for the active vs passive contrast in the left putamen and left anterior insula (A) with participant as a random factor (Z > 2.3; FWE-corrected cluster significance threshold of P < 0.05) in the mixed-effects analysis. To ensure we extracted signal change values separately for the putamen and insula, we used structurally defined regions of the putamen and insula from FSL's MNI structural atlas (B) to mask these significant clusters from the mixed-effects analysis (C). Mean percent signal change was greater in the stress condition for males and diminished in the stress condition in females in the left putamen (D) and left anterior insula (E).
We anticipated gender–stress interactions for brain activation response to reward-related decision processing in the insula, PFC and striatum. The whole-brain analysis revealed gender-by-stress interactions in the dorsal striatum (putamen) and anterior insula (Figure 4A–C). We examined the direction of effects in these ROIs by extracting mean percent signal change values by group for the lower level contrast of active–passive. An ANOVA was performed on signal change values with gender and stress condition as between-subject factors and significant interactions were found for both the left dorsal striatum, F1,43 = 22.51, P < 0.0001 and the left anterior insula, F1,43 = 6.88, P < 0.05. Examination of group means revealed that stress increased activation in the dorsal striatum and anterior insula for males during decision making but decreased activation in these regions for females (Figure 4D and E). Dorsal striatum activation did not appear to be the result of differences in motor movements alone between the active and passive conditions (see Results in Supplementary Data). Further, an Independent Component Analysis (ICA) (Calhoun et al., 2001) was conducted to identify functional networks in the brain that were differentially involved in the active BART depending on one's gender and stress status (see Methods and Results in Supplementary Data). The ICA results largely confirm results from the whole-brain GLM and ROI analyses, suggesting that males and females generally relied on the same network of brain regions to complete the BART; but under stress, there were gender differences in the involvement of the putamen and insula in this network.
Correlations were determined for cortisol change and activation in dorsal striatum and insula ROIs across and within conditions. For males only, change in cortisol predicted activation in the dorsal striatum ROI during decision processing (R24 = 0.55, P = 0.005; all other P's > 0.05); change in cortisol did not predict insula activation for any group (Ps > 0.05). Thus, in males, higher levels of physiological stress response were associated with enhanced dorsal striatum response to reward-related decision making.
A full description of correlation analysis for behavior and ROI activation can be found in the Results in Supplementary Data. Of particular interest, there was a relationship between anterior insula ROI activation and number of balloons cashed (R23 = 0.60, P = 0.002) for the stress group. In addition, for stress males alone, analyses revealed a positive correlation for dorsal striatum ROI activation and number of balloons cashed (R12 = 0.90, P < 0.000001) and a negative correlation between dorsal striatum ROI activation and risk taking (R12 = −0.75, P = 0.005). No other significant relationships were observed within gender–stress groups.
Results
Salivary Cortisol
The cold pressor nearly doubled mean cortisol levels in stress subjects, while cortisol levels did not change in controls, F1,43 = 25.56, P = 0.000002 (Figure 2). Although mean cortisol levels were higher in males, overall, F1,43 = 5.15, P = 0.03, there were no main effects of gender on cortisol change, F1,43 < 1, nor was there a gender-by-stress condition interaction, F1,43 < 1. The effect of the stressor on cortisol elevation remained highly significant after excluding participants from the analysis who did not complete the full 3-min cold pressor challenge (see Results in Supplementary Data). These results indicate that the cold pressor reliably elevated cortisol levels without significant gender-specific effects.
(Enlarge Image)
Figure 2.
Cortisol levels increased significantly in the stress group (cold pressor) but not in the control group (warm water). Cortisol responses to stress were not dependent on gender. Poststress cortisol is the average of cortisol at 21 and 35 min after the start of the hand immersion task (s2, s3, respectively); immediately before and just after the decision task. Error bars represent s.e.m.
Subjective Stress: Hand Immersion Task
Postexperiment ratings of stress resulting from the hand immersion task indicated that subjective stress experienced by participants in the cold pressor group was greater than that experienced by the control group, F1,43 = 231.75, P < 0.000001 (Mstress = 5.11 ± 1.41; Mcontrol = 1.04 ± 0.21). Subjective responses to the cold pressor were greater in women than in men, F1,43 = 4.57, P = 0.04 (Mwomen = 5.73 ± 0.91; Mmen = 4.50 ± 1.57), with no gender differences in the control group (Mwomen = 1.0 ± 0.00; Mmen = 1.08 ± 0.29), resulting in a gender-by-stress interaction, F1,43 = 6.00, P = 0.02. Additional analyses indicated that gender differences in stress-modulated decision processing were not simply the result of greater subjective stress response in females compared with males (see Results in Supplementary Data).
Behavioral Data
Consistent with our previous behavioral findings (Lighthall et al., 2009), BART behavior and earnings were similar for males and females under control conditions, but diverged with stress, leading to a gender-by-stress interaction. As displayed in Figure 3, stress increased gender differences in reward collection rate (mean number of balloons 'cashed out'), F1,43 = 4.82, P = 0.03, decision speed (button pressing intervals), F1,43 = 4.79, P = 0.03 and total earnings, F1,43 = 7.93, P = 0.007. Examination of confidence intervals indicated no gender differences in these outcome measures in the control condition, only in the stress condition. While gender-by-stress interactions were observed for these measures, individual cortisol change values were not correlated with any of the behavioral outcomes across conditions or within any groups (P's > 0.05). Regarding our measure of risk taking (mean number of pumps per balloon for nonexploding balloons), we did not find any differences by stress condition, F1,43 < 1, gender, F1,43 < 1, nor was there a gender-by-stress interaction, F1,43 < 1. Relative to the number of pumps possible per balloon (maximum = 90), the average number of pumps was fairly low across groups (M = 19.39 ± 2.38), indicating low risk taking overall. As the likelihood of losses ('explosions') during the BART increased with the number of pumps per balloon, the average number of explosions experienced per block was also low across conditions (M = 2.59 ± 0.31). There were no significant group differences or interactions in the number of explosions per block (P's > 0.05); as may be expected given the low number of pumps per balloon on average.
(Enlarge Image)
Figure 3.
Gender-by-stress effects on behavior and earnings in the BART. Group means for number of balloons completed per active block (A), decision speed (B) and total earnings in US dollars across all four active blocks (C). Error bars represent s.e.m.
While risk taking was not modulated by gender or stress in this study, our fMRI-adapted BART differed from the original task (Lejuez et al., 2002) in that the number of balloons played was only limited by the duration of active blocks. This introduced a potentially successful strategy—not present in the original BART—of playing as many balloons as quickly as possible in order to earn more money. Notably, Pearson's correlations confirmed that balloon count and decision speed were related to earnings (R47 = 0.33, P = 0.03; R47 = −0.76, P < 0.000001, respectively). Direction of stress effects by gender indicated that, from an earnings standpoint, stress led to more profitable decision behavior in males but less profitable behavior in females
See Supplementary Data in the Results section for 'Subjective stress: Scan session and BART effort'.
Whole-brain Analyses
As expected, decision-related activation (active–passive contrast) across groups was observed in regions associated with motivation and decision making. In particular, the decision task resulted in robust activation of the thalamus, putamen, caudate, anterior cingulate, dorsolateral and ventrolateral PFC, insula, inferior parietal lobe and inferior frontal gyrus. Significant clusters were also apparent in sensorimotor and visual structures (Supplementary Table S1). Further details on passive task-related activation and group differences by gender and stress can be found in Results in Supplementary Data. Of primary interest, group level analysis of decision-related activation revealed gender-by-stress interactions in motivation and decision regions; most notably in the left dorsal striatum (putamen) and left anterior insula (Figure 4 and Table 1). Gender–stress interactions were also apparent in sensorimotor and visual regions.
(Enlarge Image)
Figure 4.
Whole-brain analysis revealed significant gender–stress interactions for the active vs passive contrast in the left putamen and left anterior insula (A) with participant as a random factor (Z > 2.3; FWE-corrected cluster significance threshold of P < 0.05) in the mixed-effects analysis. To ensure we extracted signal change values separately for the putamen and insula, we used structurally defined regions of the putamen and insula from FSL's MNI structural atlas (B) to mask these significant clusters from the mixed-effects analysis (C). Mean percent signal change was greater in the stress condition for males and diminished in the stress condition in females in the left putamen (D) and left anterior insula (E).
ROI Analyses
We anticipated gender–stress interactions for brain activation response to reward-related decision processing in the insula, PFC and striatum. The whole-brain analysis revealed gender-by-stress interactions in the dorsal striatum (putamen) and anterior insula (Figure 4A–C). We examined the direction of effects in these ROIs by extracting mean percent signal change values by group for the lower level contrast of active–passive. An ANOVA was performed on signal change values with gender and stress condition as between-subject factors and significant interactions were found for both the left dorsal striatum, F1,43 = 22.51, P < 0.0001 and the left anterior insula, F1,43 = 6.88, P < 0.05. Examination of group means revealed that stress increased activation in the dorsal striatum and anterior insula for males during decision making but decreased activation in these regions for females (Figure 4D and E). Dorsal striatum activation did not appear to be the result of differences in motor movements alone between the active and passive conditions (see Results in Supplementary Data). Further, an Independent Component Analysis (ICA) (Calhoun et al., 2001) was conducted to identify functional networks in the brain that were differentially involved in the active BART depending on one's gender and stress status (see Methods and Results in Supplementary Data). The ICA results largely confirm results from the whole-brain GLM and ROI analyses, suggesting that males and females generally relied on the same network of brain regions to complete the BART; but under stress, there were gender differences in the involvement of the putamen and insula in this network.
Correlations were determined for cortisol change and activation in dorsal striatum and insula ROIs across and within conditions. For males only, change in cortisol predicted activation in the dorsal striatum ROI during decision processing (R24 = 0.55, P = 0.005; all other P's > 0.05); change in cortisol did not predict insula activation for any group (Ps > 0.05). Thus, in males, higher levels of physiological stress response were associated with enhanced dorsal striatum response to reward-related decision making.
Behavior and ROI Correlations
A full description of correlation analysis for behavior and ROI activation can be found in the Results in Supplementary Data. Of particular interest, there was a relationship between anterior insula ROI activation and number of balloons cashed (R23 = 0.60, P = 0.002) for the stress group. In addition, for stress males alone, analyses revealed a positive correlation for dorsal striatum ROI activation and number of balloons cashed (R12 = 0.90, P < 0.000001) and a negative correlation between dorsal striatum ROI activation and risk taking (R12 = −0.75, P = 0.005). No other significant relationships were observed within gender–stress groups.
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