Lake City j real sex man wemen

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Several studies have suggested that females and males differ in reward behaviors and their underlying neural circuitry. Whether human sex differences extend across neural and behavioral levels for both rewards and punishments remains unclear. We studied a community sample of young women and men who performed a monetary incentive task known to engage the mesoaccumbal pathway and salience network. Both stimulus salience behavioral relevance and valence win vs loss varied during the task. Behavioral, autonomic and neural sensitivity to the valence of stimuli did not differ by sex, indicating that responses to rewards vs punishments were similar in women and men.

These reveal novel and robust sex differences in reward- and punishment-related traits, Lake City j real sex man wemen, autonomic activity and neural responses. These convergent suggest a neurobehavioral basis for sexual dimorphism observed in the reward system, including reward-related disorders. Sex differences in the brain have increasingly been the subject of scientific and social debate. A National Institutes of Health policy requiring the consideration of sex differences in biomedical research has recently brought sexual dimorphism of the brain into the spotlight reference to NIH policy.

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Numerous studies of humans and other animals have reported differences in brain structure and function between the sexes Pohjalainen et al. Psychiatric disorders involving the reward system often present differently in men and women Becker et al. For example, men are more likely to participate in activities with a high risk of addiction, such as gambling or drug abuse, but women who participate in these activities may be more sensitive to drug effects and escalate to misuse more rapidly Fattore et al.

Similarly, major depression is more common in women and may present in a sex-specific manner.

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For example, depressed men report more symptoms of risk taking and impulsivity, whereas depressed women are more likely to report mood disturbance Cavanagh et al. Observations like these indicate that women and men differ in their vulnerability to reward-related disorders. A better understanding of differences in reward behavior and brain function between females and males is expected to provide insight into the underlying pathogenesis of disorders of the reward system.

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Furthermore, this knowledge may be useful to prevent these illnesses and improve treatment of both men and women. Studies of the reward system in rodents have demonstrated clear sex differences in behavior and neural function Perry et al. For example, female rats escalate cocaine self-administration more quickly than males, an effect that may depend on estrogen Lynch et al. Hormone- and drug-specific sex differences are also seen during withdrawal Carroll and Anker, ; Becker and Koob,where estrogen and progesterone levels can impact drug seeking behavior and negative affect during withdrawal.

A recent behavioral study of rodents found that reward-guided learning and cognitive flexibility were similar between males and females, but females learned more rapidly to avoid punishment and were more sensitive to unpredictable negative outcomes Chowdhury et al. These behavioral differences are accompanied by neural differences between males and females. Lake City j real sex man wemen example, females have lower dopamine levels in the nucleus accumbens NAclower striatal D1 receptor expression and a different pattern of striatal activation to amphetamine Becker, ; Becker and Koob, Thus, studies of animal models have demonstrated neurobehavioral differences between females and males, some of which depend on the valence of incentives reward vs punishment.

Sex differences in the human reward system have been evaluated in neuroimaging studies using a variety of methods, and the findings have been mixed.

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Munro et al. Curtis et al. In contrast, women showed a greater response than men in the NAc in response to hedonic foods when fasting, but not in a fed state Legget et al.

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Other studies reported no ificant sex differences in the NAc during reward tasks Dreher et al. Early studies were limited by small sample sizes, and most studies did not test negative-valence stimuli e. Analysis of both gain and loss is needed to clarify whether sex differences are specific to rewards or rather generalize to salient stimuli regardless of valence. Furthermore, few reports investigating sex differences in the reward system have included task-relevant performance or subjective ratings.

Thus, the behavioral impact of any neural sex differences remains largely unknown. Here we addressed the limitations of studies by examining sex differences in reward function in a large community sample of young adults. Our objective was to create a more comprehensive picture of sex differences by examining responses to both positive- and negative-valence cues rewards and losses across multiple levels of analysis: subjective ratings of incentive stimuli, task performance, autonomic arousal during the task and neural responses.

Subjective ratings provide insight into how men and women differentially perceive incentive stimuli, while task performance represents quantifiable behavior when presented with potential rewards and losses. Autonomic function, measured via skin conductance response SCRgives an objective indicator of sex differences in arousal during the task.

Neural responses allow one to examine the brain basis of these differences in response to the task between the sexes. We used a version of the monetary incentive delay MID task that quantified anticipatory responses and allowed us to distinguish sensitivity to salience behavioral relevance vs sensitivity to valence win vs loss. This task strongly engages the mesoaccumbal pathway NAc and midbrain as well as the broader salience network, which is centered on the dorsal anterior cingulate cortex dACC Lake City j real sex man wemen anterior insula AIso those structures were examined as regions of interest Menon, ; Warthen et al.

We also measured sex differences in psychological traits related to reward and punishment sensitivity Carver and White, ; Torrubia et al. We hypothesized that women would respond less strongly to increases in stimulus salience, and more strongly to negative valence stimuli across multiple neurobehavioral levels of analysis.

Health status was self-reported, and participants were also assessed by a nurse and had vital s taken. Further details concerning MINI exclusion criteria and screening are included in the supplement. For all individuals, self-reported sex agreed with genetic sex, as determined by genotyping of blood samples see Supplementary Methods. A subset of 53 participants with specific genotypes participated in the second visit which involved functional magnetic resonance imaging fMRIand data from 44 were available for analysis after quality-control screening, as described below.

In a publication Warthen et al. Participants selected for imaging fell into one of two NPY genotype groups. Sex differences were not analyzed in the original publication. Here we report findings from the full sample of subjects across a range of outcomes: psychological traits, task performance, stimulus ratings, SCRs and fMRI responses. This task is well suited to our aims as it allows for independent variation of both valence and salience of stimuli. Details are described in the Supplement and in a report Warthen et al.

The five trial types were: high-salience and positive-valence uncertain win ; high-salience and negative-valence uncertain loss Lake City j real sex man wemen low-salience and positive-valence certain win ; low-salience and negative-valence certain loss and neutral. No money was at stake during neutral trials. The five conditions were presented in pseudo-random order with 20 repetitions per condition. After the MID task, subjects rated each cue stimulus on arousal and affect Warthen et al.

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All participants performed this task outside of the scanner, and a subset of 53 subjects performed the task during functional MRI. The task was optimized to model neural responses only during the anticipatory phase of the MID task because this is when the largest neural responses to the task occur. By de, the trial duration was as short as possible so that more repetitions of each trial type could be acquired, improving the al-to-noise ratio, and therefore the target and feedback phases of this task were not variable enough in timing to model independently.

After the quality-control step see supplementdata from subjects were available for analysis. SCR z-scores were calculated as the mean peak-to-peak value divided by the peak-to-peak standard deviation across 20 repetitions of each task condition. Because the distribution of z-scores was skewed, log10 transformed SCR Lake City j real sex man wemen were used for statistical analyses. Further methodological details are provided in the Supplementary Methods.

See supplement for imaging details. Data from 44 subjects were available for analysis after quality-control procedures. Those 44 participants were similar to the remainder of the sample on demographic, physiological and clinical variables see Supplementary Material and Supplementary Table S1. The primary regions of interest in this study were selected a priori based on their known involvement in reward-related behavior and their engagement during the MID task.

The mesoaccumbal pathway includes projections of dopaminergic neurons from the midbrain ventral tegmentum and substantia nigra pars compacta to the bilateral NAc. In addition to these subcortical structures, the MID task activates the major cortical nodes of the salience network, viz. These regions were anatomically defined based on independent, ly published data see Supplementary Methods and Supplementary Figure S1. The AI was divided into dorsal and ventral subregions Gorgolewski et al.

BOLD contrast values were extracted from voxel-wise fMRI contrast images, spatially averaged across each region Lake City j real sex man wemen interest, and analyzed with linear models as described below. Analyses were performed in R version 3.

Each response measure was calculated per task condition as the mean value relative to the mean of all neutral trials high-salience win minus neutral, high-salience loss minus neutral, etc.

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Fixed-effect predictors included stimulus salience high or lowstimulus valence win or loss and salience-by-valence interaction. Because imaged subjects fell into one of two predefined genotype groups, and genotype group did influence NAc and midbrain responses [High or Low NPY expression, see Supplementary Methods and Warthen et al. Sex differences were tested with linear mixed models including subject as a random-effects predictor. Fixed-effect predictors included sex, salience, valence and two-way interactions. For each outcome measure accuracy, arousal ratings, affect ratings, SCRs and fMRI responsesthe effect of sex was separately analyzed for the salience contrast—defined as the sum of the two uncertain high salience conditions minus the sum of the two certain low salience conditions—and for the valence contrast—defined as the sum of the two gain conditions minus Lake City j real sex man wemen sum of the two loss conditions.

For whole-brain exploratory fMRI analyses in SPM, the false discovery rate was applied to adjust for multiple comparisons. ificance of indirect effects was tested using bootstrapping. Demographics, physiological variables and psychological measures from the sample women, men are shown in Tables 1S1 and S2. Across the entire sample, accuracy i. This was expected because on high- but not low-salience trials, subjects could win or avoid losing money by performing more accurately.

Accuracy Lake City j real sex man wemen also modulated by valence: subjects were more accurate on win vs loss trials. The effects of task condition are shown most clearly by examining salience and valence contrasts Figure 1B. A The boxplots show task accuracy i. B Accuracy data from A are replotted as salience contrast high minus low and valence contrast win minus loss.

C Arousal rating by condition, relative to neutral. D Salience and valence contrasts of arousal ratings. E Affect ratings by condition, relative to neutral. F Salience and valence contrasts of affect ratings. For all boxplots, center line is the median, box is interquartile range IQRwhiskers are 1. High-salience conditions are shown in maroon and low-salience conditions are shown Lake City j real sex man wemen blue. The salience contrast is calculated as high-salience conditions minus low-salience conditions, and the valence contrast is calculated as win conditions minus loss conditions.

After performing the task, subjects rated their arousal Figure 1C and D and affect Figure 1E and F for each stimulus type on a 1-to-5 scale see also Supplementary Figure S2. Affect ratings showed a different pattern Figure 1E and F. Skin conductance typically showed a biphasic response over the 10 s following stimulus presentation Figure 2A. A Example SCR by condition for one subject. Cue stimuli were presented at 0 s. B SCR z-values across all subjects.

C Salience and valence contrasts for the data shown in B. As ly reported Warthen et al. C NAc region of interest in yellow on an inflated brain medial view. F Dorsal AI region of interest in green on an inflated brain lateral view. I dACC region of interest in orange on an inflated brain medial view.

The salience BOLD contrast is calculated as high-salience conditions minus low-salience conditions, and the valence BOLD contrast is calculated as win conditions minus loss conditions. We found ificant sex differences in three reward-related trait questionnaires Table 1.

Consistent with reports Costa and McCrae, ; Shen et al. Summary of sex differences during the MID task. Women are shown in orange and men are shown in purple. C Affect ratings by condition, relative to neutral. D Salience and valence contrasts of affect ratings. E Accuracy by condition, relative to neutral. F Salience and valence contrasts of accuracy. G SCR amplitude z-value by condition, relative to neutral. H Salience and valence contrasts of SCR. I NAc response by condition, relative to neutral.

J Salience and valence contrasts of NAc response. K dACC response by condition, relative to neutral. L Salience and valence contrasts of dACC response. The pattern of sex differences for arousal ratings was similar to the pattern for accuracy. This indicated that men and women experienced similar differences in subjective affect between high- and low-salience trials, and between win and loss trials. Thus, sex differences observed in SCR mirrored those observed for behavioral accuracy and subjective arousal.

A linear mixed model was applied to each of five regions of interest. Compared to women, men showed greater sensitivity to stimulus salience within the mesoaccumbal pathway and salience network. We also found sex differences in the cortical nodes of the salience network.

No sex differences were found in other brain regions using whole-brain correction for multiple comparisons Supplementary Table S4. Because the behavioral, autonomic and neural outcomes we measured were intercorrelated Supplementary Figure S3we evaluated sex differences using linear mixed models in which level of analysis was added as a fixed-effect predictor. These findings confirmed that these sex differences in responsiveness to salience remained after ing for comparison of multiple correlated outcomes within and across levels of analysis.

Lake City j real sex man wemen

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