Miranda Jason A, Shepard Kathryn N, McClintock Shannon K, Liu Robert C
Department of Biology, Emory University, Atlanta, Georgia, United States of America; Center for Behavioral Neuroscience, Atlanta, Georgia, United States of America.
Department of Biology, Emory University, Atlanta, Georgia, United States of America; Center for Behavioral Neuroscience, Atlanta, Georgia, United States of America; Graduate Program in Neuroscience, Emory University, Atlanta, Georgia, United States of America.
PLoS One. 2014 Jul 3;9(7):e101630. doi: 10.1371/journal.pone.0101630. eCollection 2014.
Subcortical auditory nuclei were traditionally viewed as non-plastic in adulthood so that acoustic information could be stably conveyed to higher auditory areas. Studies in a variety of species, including humans, now suggest that prolonged acoustic training can drive long-lasting brainstem plasticity. The neurobiological mechanisms for such changes are not well understood in natural behavioral contexts due to a relative dearth of in vivo animal models in which to study this. Here, we demonstrate in a mouse model that a natural life experience with increased demands on the auditory system - motherhood - is associated with improved temporal processing in the subcortical auditory pathway. We measured the auditory brainstem response to test whether mothers and pup-naïve virgin mice differed in temporal responses to both broadband and tone stimuli, including ultrasonic frequencies found in mouse pup vocalizations. Mothers had shorter latencies for early ABR peaks, indicating plasticity in the auditory nerve and the cochlear nucleus. Shorter interpeak latency between waves IV and V also suggest plasticity in the inferior colliculus. Hormone manipulations revealed that these cannot be explained solely by estrogen levels experienced during pregnancy and parturition in mothers. In contrast, we found that pup-care experience, independent of pregnancy and parturition, contributes to shortening auditory brainstem response latencies. These results suggest that acoustic experience in the maternal context imparts plasticity on early auditory processing that lasts beyond pup weaning. In addition to establishing an animal model for exploring adult auditory brainstem plasticity in a neuroethological context, our results have broader implications for models of perceptual, behavioral and neural changes that arise during maternity, where subcortical sensorineural plasticity has not previously been considered.
传统观点认为,成年后皮层下听觉核团是没有可塑性的,这样听觉信息就能稳定地传递到更高的听觉区域。包括人类在内的各种物种的研究现在表明,长期的听觉训练可以驱动持久的脑干可塑性。由于缺乏用于研究这一现象的体内动物模型,在自然行为背景下,这种变化的神经生物学机制尚未得到很好的理解。在这里,我们在一个小鼠模型中证明,一种对听觉系统需求增加的自然生活经历——成为母亲——与皮层下听觉通路中时间处理能力的改善有关。我们测量了听觉脑干反应,以测试母亲和未生育过幼崽的处女鼠在对宽带和纯音刺激(包括在幼鼠叫声中发现的超声波频率)的时间反应上是否存在差异。母亲的早期听觉脑干反应峰值潜伏期更短,这表明听觉神经和耳蜗核具有可塑性。波IV和波V之间的峰间期更短也表明下丘具有可塑性。激素操纵表明,这些不能仅仅用母亲在怀孕和分娩期间所经历的雌激素水平来解释。相反,我们发现,与怀孕和分娩无关的照顾幼崽的经历有助于缩短听觉脑干反应潜伏期。这些结果表明,母亲环境中的听觉经历会赋予早期听觉处理可塑性,这种可塑性会持续到幼崽断奶之后。除了建立一个在神经行为学背景下探索成年听觉脑干可塑性的动物模型外,我们的研究结果对孕期出现的感知、行为和神经变化模型具有更广泛的意义,此前皮层下感觉神经可塑性在这些模型中尚未被考虑。