The dual role of dopamine in the modulation of information processing in the prefrontal cortex underlying social behavior

The dual role of dopamine in the modulation of information processing in the prefrontal cortex underlying social behavior
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多巴胺在调节社会行为背后的前额皮质信息处理中的双重作用

DOI:
10.1096/fj.202101637r
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发表时间:
2022
期刊:
The FASEB Journal
影响因子:
--
通讯作者:
Nawa Hiroyuki
Nawa Hiroyuki
中科院分区:
--
文献类型:
--
作者:
Sotoyama Hidekazu;Inaba Hiroyoshi;Iwakura Yuriko;Namba Hisaaki;Takei Nobuyuki;Sasaoka Toshikuni;Nawa Hiroyuki

文献摘要

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前额叶皮层中的多巴胺对社会行为的调节至关重要。然而,压力导致的社交退缩也会促进前额叶皮层中多巴胺的释放。因此,这些证据表明多巴胺在前额叶皮质中具有相反的功能。然而,多巴胺对前额叶功能的影响尚未完全了解。在这里,我们表明,多巴胺差异调制的神经元活动所引发的社会刺激在前额叶皮层,这取决于多巴胺激活(短暂或持续激活)的持续时间。使用化学发生技术,我们发现,社会行为是负调节的持续增加多巴胺神经元活性在腹侧被盖区,而它是积极的调节急性增加。社会交往的持续时间与前额叶皮层中由社会刺激引发的短暂多巴胺释放呈正相关,与前额叶多巴胺水平的持续增加呈负相关。此外,由社会刺激引发的前额叶皮层神经钙信号的升高会被前额叶多巴胺水平的持续升高所减弱,而多巴胺水平的急性升高会增强它。此外,多巴胺的慢性过量抑制了由社会刺激引发的表达多巴胺D1受体的前额叶神经元中的c-Fos诱导,而不是D2受体。这些结果表明,持续激活前额叶多巴胺,在相反的短暂激活,可以减少与社会行为相关的前额叶活动,即使是相同的多巴胺浓度。因此,多巴胺在调节前额叶活动中起着相反的作用,这取决于其作用的持续时间。
Dopamine in the prefrontal cortex is essential for the regulation of social behavior. However, stress‐causing social withdrawal also promotes dopamine release in the prefrontal cortex. Thus, this evidence suggests opposite functions of dopamine in the prefrontal cortex. However, the influence of dopamine on prefrontal functions is yet to be fully understood. Here, we show that dopamine differentially modulated the neuronal activity triggered by social stimuli in the prefrontal cortex, depending on the duration of the dopamine activation (transient or sustained activation). Using chemogenetic techniques, we have found that social behavior was negatively regulated by a sustained increase in dopamine neuronal activity in the ventral tegmental area, while it was positively regulated by an acute increase. The duration of social interactions was positively correlated with the transient dopamine release triggered by social stimuli in the prefrontal cortex and negatively correlated with the sustained increase in prefrontal dopamine levels. Furthermore, the elevation of neural calcium signal, triggered by social stimuli, in the prefrontal cortex was attenuated by the persistent elevation of prefrontal dopamine levels, whereas an acute increase in dopamine levels enhanced it. Additionally, the chronic excess of dopamine suppressed c‐Fos induction triggered by social stimuli in prefrontal neurons expressing dopamine D1 receptors, but not D2 receptors. These results suggest that sustained activation of prefrontal dopamine, at the opposite of its transient activation, can reduce prefrontal activity associated with social behavior, even for identical dopamine concentrations. Thus, dopamine plays opposite roles in modulating prefrontal activity depending on the duration of its action.