In social animals, the behavioral and hormonal responses to stress can be transmitted from one individual to another through a social transmission process, and, conversely, social support ameliorates stress responses, a phenomenon referred to as social buffering. Metaplasticity represents activity-dependent synaptic changes that modulate the ability to elicit subsequent synaptic plasticity. Authentic stress can induce hippocampal metaplasticity, but whether transmitted stress has the same ability remains unknown. Here, using an acute restraint–tailshock stress paradigm, we report that both authentic and transmitted stress in adult male mice trigger metaplastic facilitation of long-term depression (LTD) induction at hippocampal CA1 synapses. Using LTD as a readout of persistent synaptic consequences of stress, our findings demonstrate that, in a male–male dyad, stress transmission happens in nearly half of naive partners and stress buffering occurs in approximately half of male stressed mice that closely interact with naive partners. By using a social-confrontation tube test to assess the dominant–subordinate relationship in a male–male dyad, we found that stressed subordinate mice are not buffered by naive dominant partners and that stress transmission is exhibited in ~60% of dominant naive partners. Furthermore, the appearance of stress transmission correlates with more time spent in sniffing the anogenital area of stressed mice, and the appearance of stress buffering correlates with more time engaged in allogrooming from naive partners. Chemical ablation of the olfactory epithelium with dichlobenil or physical separation between social contacts diminishes stress transmission. Together, our data demonstrate that transmitted stress can elicit metaplastic facilitation of LTD induction as authentic stress.

SIGNIFICANCE STATEMENT Social animals can acquire information about their environment through interactions with conspecifics. Stress can induce enduring changes in neural activity and synaptic function. Current studies are already unraveling the transmission and buffering of stress responses between individuals, but little is known about the relevant synaptic changes associated with social transmission and buffering of stress. Here, we show that authentic and transmitted stress can prime glutamatergic synapses onto hippocampal CA1 neurons to undergo long-term depression. This hippocampal metaplasticity is bufferable following social interactions with naive partners. Hierarchical status of naive partners strongly affects the social buffering effect on synaptic consequences of stress. This work provides novel insights into the conceptual framework for synaptic changes with social transmission and buffering of stress.

在群居动物中，对压力的行为和荷尔蒙反应可以通过社会传递过程从一个人传递给另一个人，相反，社会支持会改善压力反应，这种现象被称为社会缓冲。Metaplasticity 代表活动依赖的突触变化，调节引发后续突触可塑性的能力。真实的压力可以诱导海马化生，但传递的压力是否具有相同的能力仍然未知。在这里，我们使用急性束缚-尾震应激范式，报告成年雄性小鼠的真实压力和传递压力都会触发海马 CA1 突触长期抑制 (LTD) 诱导的化生促进。使用 LTD 作为压力持续突触后果的读数，我们的研究结果表明，在雄性-雄性配对中，压力传递发生在近一半的幼稚伙伴中，而压力缓冲发生在与幼稚伙伴密切互动的大约一半雄性压力小鼠中。通过使用社会对抗管测试来评估男性 - 男性二元组中的主导 - 从属关系，我们发现压力从属的小鼠不会被幼稚的主导伙伴缓冲，并且压力传递出现在约 60% 的显性幼稚伙伴中。此外，压力传递的出现与嗅探受压小鼠的肛门生殖器区域所花费的时间更多相关，而压力缓冲的出现与更多时间参与来自幼稚伙伴的同种修饰相关。用敌草醚化学消融嗅觉上皮或在社会接触之间进行物理分离可减少压力传递。

意义声明群居动物可以通过与同种动物的互动来获取有关其环境的信息。压力会导致神经活动和突触功能的持久变化。目前的研究已经揭示了个体之间压力反应的传递和缓冲，但对与社会传递和压力缓冲相关的突触变化知之甚少。在这里，我们表明真实和传递的压力可以将谷氨酸能突触启动到海马 CA1 神经元上，从而导致长期抑郁。在与幼稚的伙伴进行社交互动后，这种海马化生是可以缓冲的。幼稚伙伴的等级地位强烈影响对压力突触后果的社会缓冲作用。