Beukema Patrick, Cecil Katherine L, Peterson Elena, Mann Victor R, Matsushita Megumi, Takashima Yoshio, Navlakha Saket, Barth Alison L
Department of Neuroscience, Center for Neuroscience at the University of Pittsburgh, Pittsburgh, Pennsylvania, 15260.
Baylor College of Medicine, Houston, Texas, 77030.
J Comp Neurol. 2018 Jun 15;526(9):1444-1456. doi: 10.1002/cne.24418. Epub 2018 Mar 25.
Somatosensation is a complex sense mediated by more than a dozen distinct neural subtypes in the periphery. Although pressure and touch sensation have been mapped to primary somatosensory cortex in rodents, it has been controversial whether pain and temperature inputs are also directed to this area. Here we use a well-defined somatosensory modality, cool sensation mediated by peripheral TrpM8-receptors, to investigate the neural substrate for cool perception in the mouse neocortex. Using activation of cutaneous TrpM8 receptor-expressing neurons, we identify candidate neocortical areas responsive for cool sensation. Initially, we optimized TrpM8 stimulation and determined that menthol, a selective TrpM8 agonist, was more effective than cool stimulation at inducing expression of the immediate-early gene c-fos in the spinal cord. We developed a broad-scale brain survey method for identification of activated brain areas, using automated methods to quantify c-fos immunoreactivity (fos-IR) across animals. Brain areas corresponding to the posterior insular cortex and secondary somatosensory (S2) show elevated fos-IR after menthol stimulation, in contrast to weaker activation in primary somatosensory cortex (S1). In addition, menthol exposure triggered fos-IR in piriform cortex, the amygdala, and the hypothalamus. Menthol-mediated activation was absent in TrpM8-knock-out animals. Our results indicate that cool somatosensory input broadly drives neural activity across the mouse brain, with neocortical signal most elevated in the posterior insula, as well as S2 and S1. These findings are consistent with data from humans indicating that the posterior insula is specialized for somatosensory information encoding temperature, pain, and gentle touch.
躯体感觉是一种复杂的感觉,由外周十几种不同的神经亚型介导。尽管在啮齿动物中,压力和触觉已被映射到初级躯体感觉皮层,但疼痛和温度输入是否也指向该区域一直存在争议。在这里,我们使用一种定义明确的躯体感觉模式,即由外周瞬时受体电位香草酸亚型8(TrpM8)受体介导的冷觉,来研究小鼠新皮层中冷觉感知的神经基础。通过激活表达皮肤TrpM8受体的神经元,我们确定了对冷觉有反应的候选新皮层区域。最初,我们优化了TrpM8刺激,并确定薄荷醇(一种选择性TrpM8激动剂)在诱导脊髓中即刻早期基因c-fos的表达方面比冷刺激更有效。我们开发了一种广泛的脑区调查方法来识别激活的脑区,使用自动化方法量化不同动物的c-fos免疫反应性(fos-IR)。与初级躯体感觉皮层(S1)中较弱的激活相比,薄荷醇刺激后,与后岛叶皮层和次级躯体感觉区(S2)相对应的脑区显示出升高的fos-IR。此外,薄荷醇暴露引发了梨状皮层、杏仁核和下丘脑的fos-IR。在TrpM8基因敲除动物中不存在薄荷醇介导的激活。我们的结果表明,冷躯体感觉输入广泛驱动小鼠大脑中的神经活动,新皮层信号在后岛叶以及S2和S1中升高最为明显。这些发现与来自人类的数据一致,表明后岛叶专门用于编码温度、疼痛和轻触觉的躯体感觉信息。