Behavioral and Transcriptomic Fingerprints of an Enriched Environment in Horses (Equus caballus)

The use of environmental enrichment (EE) has grown in popularity over decades, particularly because EE is known to promote cognitive functions and well-being. Nonetheless, little is known about how EE may affect personality and gene expression. To address this question in a domestic animal, 10-month-old horses were maintained in a controlled environment or EE for 12 weeks. The control horses (n = 9) lived in individual stalls on wood shaving bedding. They were turned out to individual paddocks three times a week and were fed three times a day with pellets or hay. EE-treated horses (n = 10) were housed in large individual stalls on straw bedding 7 hours per day and spent the remainder of the time together at pasture. They were fed three times a day with flavored pellets, hay, or fruits and were exposed daily to various objects, odors, and music. The EE modified three dimensions of personality: fearfulness, reactivity to humans, and sensory sensitivity. Some of these changes persisted >3 months after treatment. These changes are suggestive of a more positive perception of the environment and a higher level of curiosity in EE-treated horses, explaining partly why these horses showed better learning performance in a Go/No-Go task. Reduced expression of stress indicators indicated that the EE also improved well-being. Finally, whole-blood transcriptomic analysis showed that in addition to an effect on the cortisol level, the EE induced the expression of genes involved in cell growth and proliferation, while the control treatment activated genes related to apoptosis. Changes in both behavior and gene expression may constitute a psychobiological signature of the effects of enrichment and result in improved well-being. This study illustrates how the environment interacts with genetic information in shaping the individual at both the behavioral and molecular levels.环境丰容（environmental enrichment，EE）的应用在数十年间愈发普及，这主要因其已被证实可促进认知功能与机体健康福祉。然而，学界对环境丰容如何影响动物个性与基因表达的认知仍较为有限。为探究该问题在家养动物中的表现，本研究选取10月龄的马，将其分别置于对照环境与环境丰容环境中饲养12周。对照组马匹（n=9）饲养于铺有刨花垫料的单栏厩舍内，每周被牵至独立围场活动3次，每日饲喂3次，饲料为颗粒料或干草。环境丰容处理组马匹（n=10）每日有7小时被饲养于铺有稻草垫料的大型单栏厩舍，其余时间则集体在牧场活动；每日饲喂3次，饲料包括调味颗粒料、干草或水果，且每日会接触各类物品、气味与音乐。环境丰容改变了马匹个性的三个维度：恐惧性、对人类的反应性以及感官敏感性。其中部分改变在处理结束3个月后仍持续存在。这些变化表明，环境丰容处理组的马匹对环境的感知更为积极，好奇心水平更高，这在一定程度上解释了为何这些马匹在Go/No-Go任务中表现出更优的学习能力。应激指标表达量的降低表明，环境丰容还改善了马匹的健康福祉。最后，全血转录组分析显示，除了对皮质醇水平产生影响外，环境丰容还诱导了参与细胞生长与增殖的基因表达，而对照组则激活了与细胞凋亡相关的基因。行为与基因表达的改变或可构成丰容效应的心理生物学特征，并最终提升健康福祉。本研究阐明了环境如何在行为与分子层面与遗传信息相互作用，进而塑造个体。