TY - JOUR
T1 - Single-dose testosterone administration modulates instant empathic responses to others’ pain
T2 - An EEG study
AU - Zhuo, Shiwei
AU - Zhang, Wenyun
AU - Fan, Junsong
AU - Wu, Yin
AU - Wu, Wen
AU - Peng, Weiwei
N1 - Funding Information:
This study was supported by the National Natural Science Foundation of China (no. 31871127 and no. 31872784 ), the Features Innovative Projects of Guangdong Province Ordinary University (no. 2019KTSCX149 ), the Shenzhen Basic Research Project (no. 20200812113251002 ), and Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions (no. 2021SHIBS0003 ).
Publisher Copyright:
© 2022 Elsevier Ltd
PY - 2022/7
Y1 - 2022/7
N2 - Whether or not testosterone can impair empathy remains unclear in the literature. Given that empathic responses to others’ emotional experiences depend strongly upon top–down controlled mechanisms of attention, here we investigated whether the effects of testosterone administration on pain empathy could be modulated by manipulating attention. We used a double-blind, placebo-controlled within-participant design, in which either testosterone or placebo was administrated in separate sessions. Images depicting painful or nonpainful scenes were presented to induce instant empathic responses. Experiment 1 adopted the pain-judgment and hands-counting tasks to direct attention toward painful or nonpainful aspect of the images, respectively. Experiment 2 employed the pain-rating task to estimate affective and cognitive aspects of pain empathy. When discriminating nonpainful aspects of the images in the hands-counting task, accuracies were lower and empathic late positive potential responses were greater in testosterone sessions than in placebo sessions. This suggested that testosterone enhanced empathic responses to task-irrelevant pain-related features, which interfered with task performance. When providing empathic ratings to the images in the pain-rating task, empathic event-related potentials in the early stage were only observed in the testosterone session. This suggested that testosterone facilitated automatic affective reactivity to others’ pain when elaborately processing empathic stimuli. Nevertheless, when discriminating painful aspects of the images in the pain-judgment task, we did not observe any significant differences between the two sessions. These results demonstrated that testosterone effects on enhancing brain reactivity to empathic stimuli were dependent upon task demands deploying attention allocation. The enhancement likely arose from the altered brain state (e.g., increased vigilance and arousal levels) after testosterone administration, as evidenced by the reduced amplitude of spontaneous α-oscillation recorded before the onset of the images. It expands our understanding of the neurobiological mechanisms that affect empathy, and highlights the role of testosterone.
AB - Whether or not testosterone can impair empathy remains unclear in the literature. Given that empathic responses to others’ emotional experiences depend strongly upon top–down controlled mechanisms of attention, here we investigated whether the effects of testosterone administration on pain empathy could be modulated by manipulating attention. We used a double-blind, placebo-controlled within-participant design, in which either testosterone or placebo was administrated in separate sessions. Images depicting painful or nonpainful scenes were presented to induce instant empathic responses. Experiment 1 adopted the pain-judgment and hands-counting tasks to direct attention toward painful or nonpainful aspect of the images, respectively. Experiment 2 employed the pain-rating task to estimate affective and cognitive aspects of pain empathy. When discriminating nonpainful aspects of the images in the hands-counting task, accuracies were lower and empathic late positive potential responses were greater in testosterone sessions than in placebo sessions. This suggested that testosterone enhanced empathic responses to task-irrelevant pain-related features, which interfered with task performance. When providing empathic ratings to the images in the pain-rating task, empathic event-related potentials in the early stage were only observed in the testosterone session. This suggested that testosterone facilitated automatic affective reactivity to others’ pain when elaborately processing empathic stimuli. Nevertheless, when discriminating painful aspects of the images in the pain-judgment task, we did not observe any significant differences between the two sessions. These results demonstrated that testosterone effects on enhancing brain reactivity to empathic stimuli were dependent upon task demands deploying attention allocation. The enhancement likely arose from the altered brain state (e.g., increased vigilance and arousal levels) after testosterone administration, as evidenced by the reduced amplitude of spontaneous α-oscillation recorded before the onset of the images. It expands our understanding of the neurobiological mechanisms that affect empathy, and highlights the role of testosterone.
KW - Attention
KW - Empathy
KW - Event-related potentials
KW - Pain
KW - Pre-stimulus α-oscillations
KW - Testosterone
UR - http://www.scopus.com/inward/record.url?scp=85129395253&partnerID=8YFLogxK
U2 - 10.1016/j.psyneuen.2022.105768
DO - 10.1016/j.psyneuen.2022.105768
M3 - Journal article
C2 - 35500352
AN - SCOPUS:85129395253
SN - 0306-4530
VL - 141
JO - Psychoneuroendocrinology
JF - Psychoneuroendocrinology
M1 - 105768
ER -