Sex differences in brain activation to emotional stimuli: A meta-analysis of neuroimaging studies
Abstract
Substantial sex differences in emotional responses and perception have been reported in previous psychological and psychophysiological studies. For example, women have been found to respond more strongly to negative emotional stimuli, a sex difference that has been linked to an increased risk of depression and anxiety disorders. The extent to which such sex differences are reflected in corresponding differences in regional brain activation remains a largely unresolved issue, however, in part because relatively few neuroimaging studies have addressed this issue. Here, by conducting a quantitative meta-analysis of neuroimaging studies, we were able to substantially increase statistical power to detect sex differences relative to prior studies, by combining emotion studies which explicitly examined sex differences with the much larger number of studies that examined only women or men. We used an activation likelihood estimation approach to characterize sex differences in the likelihood of regional brain activation elicited by emotional stimuli relative to non-emotional stimuli. We examined sex differences separately for negative and positive emotions, in addition to examining all emotions combined. Sex differences varied markedly between negative and positive emotion studies. The majority of sex differences favoring women were observed for negative emotion, whereas the majority of the sex differences favoring men were observed for positive emotion. This valence-specificity was particularly evident for the amygdala. For negative emotion, women exhibited greater activation than men in the left amygdala, as well as in other regions including the left thalamus, hypothalamus, mammillary bodies, left caudate, and medial prefrontal cortex. In contrast, for positive emotion, men exhibited greater activation than women in the left amygdala, as well as greater activation in other regions including the bilateral inferior frontal gyrus and right fusiform gyrus. These meta-analysis findings indicate that the amygdala, a key region for emotion processing, exhibits valence-dependent sex differences in activation to emotional stimuli. The greater left amygdala response to negative emotion for women accords with previous reports that women respond more strongly to negative emotional stimuli, as well as with hypothesized links between increased neurobiological reactivity to negative emotion and increased prevalence of depression and anxiety disorders in women. The finding of greater left amygdala activation for positive emotional stimuli in men suggests that greater amygdala responses reported previously for men for specific types of positive stimuli may also extend to positive stimuli more generally. In summary, this study extends efforts to characterize sex differences in brain activation during emotion processing by providing the largest and most comprehensive quantitative meta-analysis to date, and for the first time examining sex differences as a function of positive vs. negative emotional valence. The current findings highlight the importance of considering sex as a potential factor modulating emotional processing and its underlying neural mechanisms, and more broadly, the need to consider individual differences in understanding the neurobiology of emotion.
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Previous research shows that the amygdala has different responses to positive and negative valence social information in men and women.
“Previous research has shown that the amygdala has different responses to positive and negative valence social information in men and women (11)”
From Oxytocin, the peptide that bonds the sexes also divides them (2016) · cites this paper as [11]
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Sex differences in effective fronto-limbic connectivity during negative emotion processing
Lungu, O., Potvin, S., Tikàsz, A., & Mendrek, A. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.08.012 · Cited by 96 · see citing works
Amygdala subnuclei resting-state functional connectivity sex and estrogen differences
Engman, J., Linnman, C., Van Dijk, K. R. A., & Milad, M. R. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.09.012 · Cited by 89 · see citing works
Sex differences: Transcriptional signatures of stress exposure in male and female brains
Brivio, E., Lopez, J. P., & Chen, A. (2020) · Genes, Brain and Behavior · doi:10.1111/gbb.12643 · Cited by 95 · see citing works
Helpman, L., Zhu, X., Suarez-Jimenez, B., Lazarov, A., Monk, C., & Neria, Y. (2017) · Current Psychiatry Reports · doi:10.1007/s11920-017-0854-y · Cited by 82 · see citing works
Sex differences in the functional connectivity of the amygdalae in association with cortisol
Kogler, L., Müller, V. I., Seidel, E.-M., Boubela, R., Kalcher, K., Moser, E., Habel, U., Gur, R. C., Eickhoff, S. B., & Derntl, B. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.03.064 · Cited by 78 · see citing works
Sex-dependent neural effect of oxytocin during subliminal processing of negative emotion faces.
Luo, L., Becker, B., Geng, Y., Zhao, Z., Gao, S., Zhao, W., Yao, S., Zheng, X., Ma, X., Gao, Z., et al. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.08.079 · Cited by 79 · see citing works
Sex/gender differences in cognitive abilities
Kheloui, S., Jacmin-Park, S., Larocque, O., Kerr, P., Rossi, M., Cartier, L., & Juster, R.-P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105333 · Cited by 78 · see citing works
Tiwari, A., & Gonzalez, A. (2018) · Clinical Psychology Review · doi:10.1016/j.cpr.2018.01.006 · Cited by 71 · see citing works
Sex differences in the neural correlates of affective experience
Moriguchi, Y., Touroutoglou, A., Dickerson, B. C., & Barrett, L. F. (2014) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst030 · Cited by 70 · see citing works
Gupta, A., Mayer, E. A., Acosta, J. R., Hamadani, K., Torgerson, C., van Horn, J. D., Chang, L., Naliboff, B., Tillisch, K., & Labus, J. S. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.02.003 · Cited by 56 · see citing works
Hardee, J. E., Cope, L. M., Munier, E. C., Welsh, R. C., Zucker, R. A., & Heitzeg, M. M. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx021 · Cited by 54 · see citing works
Intranasal oxytocin modulates neural functional connectivity during human social interaction
Rilling, J. K., Chen, X., Chen, X., & Haroon, E. (2018) · American Journal of Primatology · doi:10.1002/ajp.22740 · Cited by 40 · see citing works
Winter, D. (2016) · Borderline Personality Disorder and Emotion Dysregulation · doi:10.1186/s40479-016-0047-z · Cited by 36 · see citing works
Gender moderates valence effects on the late positive potential to emotional distracters
Syrjänen, E., & Wiens, S. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.07.018 · Cited by 30 · see citing works
Chen, Y.-T., Huang, M.-W., Hung, I.-C., Lane, H.-Y., & Hou, C.-J. (2014) · Behavioral and Brain Functions · doi:10.1186/1744-9081-10-36 · Cited by 24 · see citing works
Neuroanatomical correlates of perceived stress controllability in adolescents and emerging adults
Fassett-Carman, A. N., Smolker, H., Hankin, B. L., Snyder, H. R., & Banich, M. T. (2022) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-022-00985-2 · Cited by 14 · see citing works
Emotional context restores cortical prediction error responses in schizophrenia
Vogel, B. O., Stasch, J., Walter, H., & Neuhaus, A. H. (2018) · Schizophrenia Research · doi:10.1016/j.schres.2018.02.030 · Cited by 10 · see citing works
- Authors
- Stevens, J. S., & Hamann, S.
- Affiliations
- Emory University (US)
- Corresponding author
- Hamann, Stephan
- Venue
- Neuropsychologia
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 50
- Issue
- 7
- Pages
- 1578-1593
- ISSN
- 0028-3932 (ISSN-L)
- OpenAlex
- W2134534003
- Cited by
- 588
- References
- 83
- Citations by year
- 2026: 33 · 2025: 45 · 2024: 35 · 2023: 34 · 2022: 44 · 2021: 38 · 2020: 82 · 2019: 48 · 2018: 43 · 2017: 42 · 2016: 35 · 2015: 39 · 2014: 26 · 2013: 35 · 2012: 9
- FWCI
- 2.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuropsychologia (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Sex and Gender in Healthcare
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Keywords
- sex differences, emotional processing, brain activation, amygdala, emotional valence, negative emotions, positive emotions, activation likelihood estimation, thalamus, hypothalamus, mammillary bodies, caudate nucleus, medial prefrontal cortex, inferior frontal gyrus, fusiform gyrus, depression, anxiety disorders
- MeSH terms
- Brain, Brain Mapping, Emotions, Female, Humans, Male, Pattern Recognition, Visual, Photic Stimulation, Sex Characteristics, Neuroimaging
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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