Vanderbilt University Institute of Imaging Science, and Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, Tennessee 37232.
Vanderbilt University Institute of Imaging Science, and Department of Radiology and Radiological Sciences, Vanderbilt University Medical Center, Nashville, Tennessee 37232
J Neurosci. 2018 Feb 14;38(7):1774-1787. doi: 10.1523/JNEUROSCI.2795-17.2017. Epub 2018 Jan 15.
This study addresses one long-standing question of whether functional separations are preserved for somatosensory modalities of touch, heat, and cold nociception within primate primary somatosensory (S1) cortex. This information is critical for understanding how the nature of pain is represented in the primate brain. Using a combination of submillimeter-resolution fMRI and microelectrode local field potential (LFP) and spike recordings, we identified spatially segregated cortical zones for processing touch and nociceptive heat and cold stimuli in somatotopically appropriate areas 3a, 3b, 1, and 2 of S1 in male monkeys. The distances between zones were comparable (∼3.4 mm) across stimulus modalities (heat, cold, and tactile), indicating the existence of uniform, modality-specific modules. Stimulus-evoked LFP maps validated the fMRI maps in areas 3b and 1. Isolation of heat and cold nociceptive neurons from the fMRI zones confirmed the validity of using fMRI to probe nociceptive regions and circuits. Resting-state fMRI analysis revealed distinct intrinsic functional circuits among functionally related zones. We discovered distinct modular structures and networks for thermal nociception within S1 cortex, a finding that has significant implications for studying chronic pain syndromes and guiding the selection of neuromodulation targets for chronic pain management. Primate S1 subregions contain discrete heat and cold nociceptive modules. Modules with the same properties exhibit strong functional connection. Nociceptive fMRI response coincides with LFP and spike activities of nociceptive neurons. Functional separation of heat and cold pain is retained within primate S1 cortex.
本研究解决了一个长期存在的问题，即在灵长类动物初级体感皮层（S1）中，触摸、热和冷伤害感受等体感模态的功能分离是否得到保留。这一信息对于理解疼痛的性质在灵长类动物大脑中是如何表现的至关重要。本研究使用亚毫米分辨率 fMRI 和微电极局部场电位（LFP）和尖峰记录的组合，在雄性猴子的 S1 的体感区域 3a、3b、1 和 2 中，鉴定出了用于处理触摸和伤害性热冷刺激的空间分离的皮质区。各刺激模态（热、冷和触觉）之间的区带距离相当（约 3.4mm），表明存在统一的、模态特异性的模块。LFP 图谱刺激验证了 fMRI 图谱在 3b 和 1 区的有效性。从 fMRI 区分离伤害性热和冷神经元证实了使用 fMRI 探测伤害性区域和回路的有效性。静息态 fMRI 分析揭示了功能相关区之间存在独特的内在功能回路。我们发现 S1 皮层内的热伤害感受具有独特的模块结构和网络，这一发现对研究慢性疼痛综合征和指导慢性疼痛管理的神经调节靶点选择具有重要意义。灵长类 S1 亚区包含离散的热和冷伤害感受模块。具有相同特性的模块表现出强烈的功能连接。伤害感受 fMRI 反应与伤害感受神经元的 LFP 和尖峰活动一致。灵长类 S1 皮层内保留了热和冷痛的功能分离。
