Kahan Anat, Ben-Shaul Yoram
Department of Medical Neurobiology, Hebrew University Medical School, Jerusalem, Israel.
PLoS Comput Biol. 2016 Mar 3;12(3):e1004798. doi: 10.1371/journal.pcbi.1004798. eCollection 2016 Mar.
For many animals, chemosensation is essential for guiding social behavior. However, because multiple factors can modulate levels of individual chemical cues, deriving information about other individuals via natural chemical stimuli involves considerable challenges. How social information is extracted despite these sources of variability is poorly understood. The vomeronasal system provides an excellent opportunity to study this topic due to its role in detecting socially relevant traits. Here, we focus on two such traits: a female mouse's strain and reproductive state. In particular, we measure stimulus-induced neuronal activity in the accessory olfactory bulb (AOB) in response to various dilutions of urine, vaginal secretions, and saliva, from estrus and non-estrus female mice from two different strains. We first show that all tested secretions provide information about a female's receptivity and genotype. Next, we investigate how these traits can be decoded from neuronal activity despite multiple sources of variability. We show that individual neurons are limited in their capacity to allow trait classification across multiple sources of variability. However, simple linear classifiers sampling neuronal activity from small neuronal ensembles can provide a substantial improvement over that attained with individual units. Furthermore, we show that some traits are more efficiently detected than others, and that particular secretions may be optimized for conveying information about specific traits. Across all tested stimulus sources, discrimination between strains is more accurate than discrimination of receptivity, and detection of receptivity is more accurate with vaginal secretions than with urine. Our findings highlight the challenges of chemosensory processing of natural stimuli, and suggest that downstream readout stages decode multiple behaviorally relevant traits by sampling information from distinct but overlapping populations of AOB neurons.
对于许多动物而言,化学感应对于引导社会行为至关重要。然而,由于多种因素可调节个体化学信号的水平,通过自然化学刺激获取有关其他个体的信息面临诸多挑战。尽管存在这些变异性来源,但社会信息是如何被提取的,目前还知之甚少。犁鼻系统因其在检测与社会相关特征方面的作用,为研究这一课题提供了绝佳机会。在此,我们聚焦于两个此类特征:雌性小鼠的品系和生殖状态。具体而言,我们测量了副嗅球(AOB)中刺激诱导的神经元活动,以响应来自两种不同品系的发情期和非发情期雌性小鼠的尿液、阴道分泌物和唾液的各种稀释液。我们首先表明,所有测试的分泌物都提供了有关雌性接受性和基因型的信息。接下来,我们研究了尽管存在多种变异性来源,但如何从神经元活动中解码这些特征。我们表明,单个神经元在跨多种变异性来源进行特征分类的能力上是有限的。然而,从小神经元集合中采样神经元活动的简单线性分类器,相比单个神经元能有显著改进。此外,我们表明某些特征比其他特征能更有效地被检测到,并且特定的分泌物可能针对传达特定特征的信息进行了优化。在所有测试的刺激源中,品系间的区分比接受性的区分更准确,并且阴道分泌物检测接受性比尿液更准确。我们的研究结果凸显了自然刺激化学感应处理的挑战,并表明下游读出阶段通过从AOB神经元的不同但重叠群体中采样信息来解码多种与行为相关的特征。