Cortical Amygdala Consolidates a Socially Transmitted Long-Term Memory

Social communication guides decision making that is essential for survival. Social transmission of food preference (STFP) is an ecologically relevant memory paradigm in which an animal learns a desirable food odor from other animals. How food-preference memory is acquired, consolidated, and stored is unclear. Here, we identify a circuit involving the posteromedial nucleus of the cortical amygdala (COApm) as a computational center that integrates social and sensory olfactory inputs for long-term STFP memory consolidation. Blocking synaptic signaling by the COApm circuit selectively abolished STFP memory consolidation without impairing memory acquisition, storage, or recall. STFP memory consolidation by the COApm depended on synaptic inputs from the accessory olfactory bulb and synaptic outputs to the anterior olfactory nucleus and required protein synthesis, suggesting a gene expression mechanism. Deep single-cell and spatial transcriptomics revealed robust but distinct gene expression signatures induced by STFP memory formation in the COApm consistent with synapse restructuring. Our data thus define a neural circuit for consolidation of a socially communicated long-term memory, thereby mechanistically distinguishing protein synthesis-dependent memory consolidation from memory acquisition, storage, or retrieval.

社会交往介导的决策是生存所必需的。食物偏好社会传递（Social transmission of food preference, STFP）是一种具有生态学相关性的记忆范式，指动物从同类个体处习得合意的食物气味。目前学界对食物偏好记忆的获取、巩固与存储机制仍不明确。本研究鉴定出一条以皮层杏仁核后内侧亚核（posteromedial nucleus of the cortical amygdala, COApm）为计算中枢的神经环路，该环路可整合社会与嗅觉感觉输入，参与长期食物偏好社会传递记忆的巩固过程。阻断该亚核环路的突触信号传递，可选择性消除食物偏好社会传递记忆的巩固，却不影响记忆的获取、存储与提取。皮层杏仁核后内侧亚核介导的食物偏好社会传递记忆巩固依赖于副嗅球的突触输入与向前嗅核的突触输出，且需要蛋白质合成，提示存在基因表达调控机制。深度单细胞与空间转录组学分析显示，在食物偏好社会传递记忆形成过程中，皮层杏仁核后内侧亚核内诱导产生的基因表达特征显著且独特，与突触重构过程相符。综上，本研究明确了一条介导社会传递型长期记忆巩固的神经环路，从机制上将依赖蛋白质合成的记忆巩固过程与记忆的获取、存储及提取区分开来。