François Amaury, Low Sarah A, Sypek Elizabeth I, Christensen Amelia J, Sotoudeh Chaudy, Beier Kevin T, Ramakrishnan Charu, Ritola Kimberly D, Sharif-Naeini Reza, Deisseroth Karl, Delp Scott L, Malenka Robert C, Luo Liqun, Hantman Adam W, Scherrer Grégory
Department of Anesthesiology, Perioperative and Pain Medicine, Department of Molecular and Cellular Physiology, Department of Neurosurgery, Stanford Neurosciences Institute, Stanford University, Stanford, CA 94305, USA.
Department of Electrical Engineering, Stanford University, Stanford, CA 94305, USA.
Neuron. 2017 Feb 22;93(4):822-839.e6. doi: 10.1016/j.neuron.2017.01.008. Epub 2017 Feb 2.
Pain thresholds are, in part, set as a function of emotional and internal states by descending modulation of nociceptive transmission in the spinal cord. Neurons of the rostral ventromedial medulla (RVM) are thought to critically contribute to this process; however, the neural circuits and synaptic mechanisms by which distinct populations of RVM neurons facilitate or diminish pain remain elusive. Here we used in vivo opto/chemogenetic manipulations and trans-synaptic tracing of genetically identified dorsal horn and RVM neurons to uncover an RVM-spinal cord-primary afferent circuit controlling pain thresholds. Unexpectedly, we found that RVM GABAergic neurons facilitate mechanical pain by inhibiting dorsal horn enkephalinergic/GABAergic interneurons. We further demonstrate that these interneurons gate sensory inputs and control pain through temporally coordinated enkephalin- and GABA-mediated presynaptic inhibition of somatosensory neurons. Our results uncover a descending disynaptic inhibitory circuit that facilitates mechanical pain, is engaged during stress, and could be targeted to establish higher pain thresholds. VIDEO ABSTRACT.
痛阈部分是由脊髓中伤害性感受传递的下行调节作为情绪和内部状态的函数来设定的。延髓头端腹内侧(RVM)的神经元被认为对这一过程有至关重要的作用;然而,不同群体的RVM神经元促进或减轻疼痛的神经回路和突触机制仍然不清楚。在这里,我们使用体内光/化学遗传学操作以及对基因鉴定的背角和RVM神经元进行跨突触追踪,以揭示一个控制痛阈的RVM-脊髓-初级传入神经回路。出乎意料的是,我们发现RVMγ-氨基丁酸能神经元通过抑制背角脑啡肽能/γ-氨基丁酸能中间神经元来促进机械性疼痛。我们进一步证明,这些中间神经元通过脑啡肽和γ-氨基丁酸介导的体感神经元突触前抑制的时间协调来控制感觉输入并控制疼痛。我们的结果揭示了一个促进机械性疼痛、在应激期间起作用并且可以作为提高痛阈靶点的下行双突触抑制回路。视频摘要。