{"title":"The role of testosterone in modulating positive and negative empathy in social interactions","authors":"Shiwei Zhuo , Yinhua Zhang , Chennan Lin , Wen Wu , Weiwei Peng","doi":"10.1016/j.neuropharm.2025.110465","DOIUrl":null,"url":null,"abstract":"<div><div>Empathy encompasses both negative (e.g., distress) and positive (e.g., shared joy) dimensions, yet the effects of testosterone on positive empathy and its modulation of intrinsic neural dynamics remain underexplored. This double-blind, placebo-controlled study examined how testosterone influences neural sensitivity to empathy within social inclusion and exclusion contexts, as well as its impact on resting-state EEG microstates—millisecond-scale transient patterns of brain activity. Healthy male participants received either testosterone or placebo before completing resting-state EEG recordings and an empathy task featuring social scenarios. While self-reported empathy ratings remained unchanged, testosterone amplified neurophysiological responses: it enhanced anterior N2 amplitude (250–310 ms), associated with negative empathy toward social exclusion, and increased posterior α-event-related desynchronization (8.28–10 Hz; 1226–1901 ms), linked to positive empathy during social inclusion. These findings suggest that testosterone enhances neural responsiveness to both threatening and affiliative social cues, reinforcing its role in adaptive social vigilance. Resting-state EEG microstate analysis further revealed that testosterone prolonged the temporal dominance of microstate E—a centro-parietal activity pattern associated with interoceptive awareness and emotional processing. Notably, these microstate E changes predicted increased emotional empathy across both positive and negative contexts. Together, our findings suggest that testosterone indirectly enhances empathy-related responsiveness by amplifying baseline interoceptive sensitivity to socially salient stimuli. These dual effects—enhanced intrinsic interoceptive processing and heightened neural reactivity to social cues—position testosterone as a key neuromodulator of context-adaptive social perception.</div></div>","PeriodicalId":19139,"journal":{"name":"Neuropharmacology","volume":"274 ","pages":"Article 110465"},"PeriodicalIF":4.6000,"publicationDate":"2025-04-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuropharmacology","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0028390825001716","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Empathy encompasses both negative (e.g., distress) and positive (e.g., shared joy) dimensions, yet the effects of testosterone on positive empathy and its modulation of intrinsic neural dynamics remain underexplored. This double-blind, placebo-controlled study examined how testosterone influences neural sensitivity to empathy within social inclusion and exclusion contexts, as well as its impact on resting-state EEG microstates—millisecond-scale transient patterns of brain activity. Healthy male participants received either testosterone or placebo before completing resting-state EEG recordings and an empathy task featuring social scenarios. While self-reported empathy ratings remained unchanged, testosterone amplified neurophysiological responses: it enhanced anterior N2 amplitude (250–310 ms), associated with negative empathy toward social exclusion, and increased posterior α-event-related desynchronization (8.28–10 Hz; 1226–1901 ms), linked to positive empathy during social inclusion. These findings suggest that testosterone enhances neural responsiveness to both threatening and affiliative social cues, reinforcing its role in adaptive social vigilance. Resting-state EEG microstate analysis further revealed that testosterone prolonged the temporal dominance of microstate E—a centro-parietal activity pattern associated with interoceptive awareness and emotional processing. Notably, these microstate E changes predicted increased emotional empathy across both positive and negative contexts. Together, our findings suggest that testosterone indirectly enhances empathy-related responsiveness by amplifying baseline interoceptive sensitivity to socially salient stimuli. These dual effects—enhanced intrinsic interoceptive processing and heightened neural reactivity to social cues—position testosterone as a key neuromodulator of context-adaptive social perception.
移情包括消极(如痛苦)和积极(如分享快乐)两个方面,但睾酮对积极移情的影响及其对内在神经动态的调节作用仍未得到充分探索。这项双盲安慰剂对照研究考察了睾酮如何影响神经系统在社会包容和排斥背景下对移情的敏感性,以及睾酮对静息态脑电图微态--毫秒级瞬时大脑活动模式--的影响。健康男性参与者在完成静息态脑电记录和以社会情景为特色的移情任务之前,会接受睾酮或安慰剂治疗。睾酮增强了前N2振幅(250-310毫秒),这与对社会排斥的负移情有关;睾酮增强了后α事件相关非同步化(8.28-10赫兹;1226-1901毫秒),这与社会包容过程中的正移情有关。这些研究结果表明,睾酮能增强神经对威胁性和附属性社会线索的反应能力,从而加强其在适应性社会警觉中的作用。静息态脑电图微态分析进一步显示,睾酮延长了微态E的时间优势--微态E是顶叶中央的一种活动模式,与内感知意识和情绪处理有关。值得注意的是,这些微态 E 的变化预示着情感共鸣在积极和消极情境中都会增加。总之,我们的研究结果表明,睾酮通过放大对社会显著刺激的基线内感知敏感性,间接增强了与移情相关的反应能力。这些双重效应--增强内在感受性处理和提高对社会线索的神经反应--将睾酮定位为情境适应性社会感知的关键神经调节器。
期刊介绍:
Neuropharmacology publishes high quality, original research and review articles within the discipline of neuroscience, especially articles with a neuropharmacological component. However, papers within any area of neuroscience will be considered. The journal does not usually accept clinical research, although preclinical neuropharmacological studies in humans may be considered. The journal only considers submissions in which the chemical structures and compositions of experimental agents are readily available in the literature or disclosed by the authors in the submitted manuscript. Only in exceptional circumstances will natural products be considered, and then only if the preparation is well defined by scientific means. Neuropharmacology publishes articles of any length (original research and reviews).