Animal behaviours that are superficially similar can express different intents in different contexts, but how this flexibility is achieved at the level of neural circuits is not understood. For example, males of many species can exhibit mounting behaviour towards same- or opposite-sex conspecifics 1 , but it is unclear whether the intent and neural encoding of these behaviours are similar or different. Here we show that female- and male-directed mounting in male laboratory mice are distinguishable by the presence or absence of ultrasonic vocalizations (USVs) 2 – 4 , respectively. These and additional behavioural data suggest that most male-directed mounting is aggressive, although in rare cases it can be sexual. We investigated whether USV + and USV − mounting use the same or distinct hypothalamic neural substrates. Micro-endoscopic imaging of neurons positive for oestrogen receptor 1 (ESR1) in either the medial preoptic area (MPOA) or the ventromedial hypothalamus, ventrolateral subdivision (VMHvl) revealed distinct patterns of neuronal activity during USV + and USV − mounting, and the type of mounting could be decoded from population activity in either region. Intersectional optogenetic stimulation of MPOA neurons that express ESR1 and vesicular GABA transporter (VGAT) (MPOA ESR1∩VGAT neurons) robustly promoted USV + mounting, and converted male-directed attack to mounting with USVs. By contrast, stimulation of VMHvl neurons that express ESR1 (VMHvl ESR1 neurons) promoted USV − mounting, and inhibited the USVs evoked by female urine. Terminal stimulation experiments suggest that these complementary inhibitory effects are mediated by reciprocal projections between the MPOA and VMHvl. Together, these data identify a hypothalamic subpopulation that is genetically enriched for neurons that causally induce a male reproductive behavioural state, and indicate that reproductive and aggressive states are represented by distinct population codes distributed between MPOA ESR1 and VMHvl ESR1 neurons, respectively. Thus, similar behaviours that express different internal states are encoded by distinct hypothalamic neuronal populations. Ultrasonic vocalizations of male mice distinguish aggressive, male-directed mounting from reproductive, female-directed mounting behaviours, which are represented by distinct ESR1-expressing populations of neurons in the ventromedial hypothalamus and medial preoptic area, respectively.

中文翻译：

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下丘脑对小鼠同性和异性骑乘行为的独特控制


表面上相似的动物行为可以在不同的环境中表达不同的意图，但这种灵活性是如何在神经回路层面实现的尚不清楚。例如，许多物种的雄性可以对同性或异性同种动物表现出越来越多的行为 1 ，但尚不清楚这些行为的意图和神经编码是否相似或不同。在这里，我们表明，雄性实验室小鼠中的雌性和雄性定向安装可分别通过超声波发声 (USV) 2 – 4 的存在或不存在来区分。这些和其他行为数据表明，大多数男性主导的骑乘行为具有攻击性，尽管在极少数情况下可能是性行为。我们研究了 USV + 和 USV - 安装是否使用相同或不同的下丘脑神经基质。对内侧视前区 (MPOA) 或腹内侧下丘脑、腹外侧分区 (VMHvl) 雌激素受体 1 (ESR1) 阳性神经元的显微内窥镜成像揭示了 USV + 和 USV - 安装过程中神经元活动的不同模式，以及类型可以从任一地区的人口活动来解读人口增长的情况。对表达 ESR1 和囊泡 GABA 转运蛋白 (VGAT) 的 MPOA 神经元（MPOA ESR1∩VGAT 神经元）进行交叉光遗传学刺激，有力地促进了 USV + 骑乘，并将男性定向攻击转变为使用 USV 骑乘。相比之下，表达ESR1的VMHvl神经元（VMHvl ESR1神经元）的刺激促进了USV-安装，并抑制了女性尿液诱发的USV。终末刺激实验表明，这些互补的抑制作用是由 MPOA 和 VMHvl 之间的相互投射介导的。 总之，这些数据确定了一个下丘脑亚群，该亚群在基因上富集神经元，从而诱发男性生殖行为状态，并表明生殖和攻击状态分别由分布在 MPOA ESR1 和 VMHvl ESR1 神经元之间的不同群体代码表示。因此，表达不同内部状态的相似行为是由不同的下丘脑神经元群体编码的。雄性小鼠的超声波发声区分了攻击性、雄性定向的骑乘行为和生殖性、雌性定向的骑乘行为，这分别由腹内侧下丘脑和内侧视前区中不同的表达 ESR1 的神经元群体代表。