Instituto de Neurociencias, Universidad Miguel Hernández-CSIC, San Juan de Alicante, Spain.
Laboratory of Ion Channel Research, VIB-KU Leuven Center for Brain & Disease Research, Leuven, Belgium.
J Physiol. 2024 Apr;602(7):1405-1426. doi: 10.1113/JP285008. Epub 2024 Mar 8.
Ocular Surface (OS) somatosensory innervation detects external stimuli producing perceptions, such as pain or dryness, the most relevant symptoms in many OS pathologies. Nevertheless, little is known about the central nervous system circuits involved in these perceptions, and how they integrate multimodal inputs in general. Here, we aim to describe the thalamic and cortical activity in response to OS stimulation of different modalities. Electrophysiological extracellular recordings in anaesthetized rats were used to record neural activity, while saline drops at different temperatures were applied to stimulate the OS. Neurons were recorded in the ophthalmic branch of the trigeminal ganglion (TG, 49 units), the thalamic VPM-POm nuclei representing the face (Th, 69 units) and the primary somatosensory cortex (S1, 101 units). The precise locations for Th and S1 neurons receiving OS information are reported here for the first time. Interestingly, all recorded nuclei encode modality both at the single neuron and population levels, with noxious stimulation producing a qualitatively different activity profile from other modalities. Moreover, neurons responding to new combinations of stimulus modalities not present in the peripheral TG subsequently appear in Th and S1, being organized in space through the formation of clusters. Besides, neurons that present higher multimodality display higher spontaneous activity. These results constitute the first anatomical and functional characterization of the thalamocortical representation of the OS. Furthermore, they provide insight into how information from different modalities gets integrated from the peripheral nervous system into the complex cortical networks of the brain. KEY POINTS: Anatomical location of thalamic and cortical ocular surface representation. Thalamic and cortical neuronal responses to multimodal stimulation of the ocular surface. Increasing functional complexity along trigeminal neuroaxis. Proposal of a new perspective on how peripheral activity shapes central nervous system function.
眼表（OS）躯体感觉传入神经检测到外部刺激产生感觉，如疼痛或干燥，这是许多 OS 病理中最相关的症状。然而，对于涉及这些感觉的中枢神经系统回路以及它们如何整合一般的多模态输入，我们知之甚少。在这里，我们旨在描述不同模态的 OS 刺激引起的丘脑和皮质活动。在麻醉大鼠中使用电生理细胞外记录来记录神经活动，同时将不同温度的盐水滴应用于 OS 以进行刺激。在三叉神经节（TG）的眼支（49 个单位）、代表面部的丘脑 VPM-POm 核（Th，69 个单位）和初级躯体感觉皮层（S1，101 个单位）中记录神经元。这里首次报道了接收 OS 信息的 Th 和 S1 神经元的精确位置。有趣的是，所有记录的核都在单个神经元和群体水平上编码模态，有害刺激产生的活动模式与其他模态明显不同。此外，对新的刺激模态组合的反应随后出现在 Th 和 S1 中的神经元，通过形成簇在空间中组织。此外，表现出更高多模态的神经元具有更高的自发活动。这些结果构成了 OS 丘脑皮质代表的第一个解剖学和功能特征。此外，它们为我们提供了深入了解来自不同模态的信息如何从外周神经系统整合到大脑的复杂皮质网络中。关键点： 眼表的丘脑和皮质代表的解剖位置。 多模态刺激眼表时丘脑和皮质神经元的反应。 三叉神经神经轴上功能复杂性的增加。 关于外周活动如何塑造中枢神经系统功能的新视角的建议。
