Neuroimaging-based evidence for sympathetic correlation between brain activity and peripheral vasomotion during pain anticipation

• Published in: Scientific reports Vol. 14; no. 1; pp. 3383 - 14
• Main Authors: Xu, Ziqiang, Soh, Zu, Kurota, Yuta, Kimura, Yuya, Hirano, Harutoyo, Sasaoka, Takafumi, Yoshino, Atsuo, Tsuji, Toshio
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 09.02.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/378; 639/166/985; Anxiety; Brain mapping; Functional magnetic resonance imaging; Humanities and Social Sciences; Innervation; Magnetic resonance imaging; Medical imaging; multidisciplinary; Neuroimaging; Pain; Pain perception; Perception; Science; Science (multidisciplinary); Sensation; Sympathetic nervous system; Visual stimuli
• DOI: 10.1038/s41598-024-53921-4
• ISSN: 2045-2322

Anticipation of pain engenders anxiety and fear, potentially shaping pain perception and governing bodily responses such as peripheral vasomotion through the sympathetic nervous system (SNS). Sympathetic innervation of vascular tone during pain perception has been quantified using a peripheral arterial stiffness index; however, its innervation role during pain anticipation remains unclear. This paper reports on a neuroimaging-based study designed to investigate the responsivity and attribution of the index at different levels of anticipatory anxiety and pain perception. The index was measured in a functional magnetic resonance imaging experiment that randomly combined three visual anticipation cues and painful stimuli of two intensities. The peripheral and cerebral responses to pain anticipation and perception were quantified to corroborate bodily responsivity, and their temporal correlation was also assessed to identify the response attribution of the index. Contrasting with the high responsivity across levels of pain sensation, a low responsivity of the index across levels of anticipatory anxiety revealed its specificity across pain experiences. Discrepancies between the effects of perception and anticipation were validated across regions and levels of brain activity, providing a brain basis for peripheral response specificity. The index was also characterized by a 1-s lag in both anticipation and perception of pain, implying top-down innervation of the periphery. Our findings suggest that the SNS responds to pain in an emotion-specific and sensation-unbiased manner, thus enabling an early assessment of individual pain perception using this index. This study integrates peripheral and cerebral hemodynamic responses toward a comprehensive understanding of bodily responses to pain.