Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
PLoS Biol. 2022 May 6;20(5):e3001540. doi: 10.1371/journal.pbio.3001540. eCollection 2022 May.
Prediction errors (PEs) are generated when there are differences between an expected and an actual event or sensory input. The insula is a key brain region involved in pain processing, and studies have shown that the insula encodes the magnitude of an unexpected outcome (unsigned PEs). In addition to signaling this general magnitude information, PEs can give specific information on the direction of this deviation-i.e., whether an event is better or worse than expected. It is unclear whether the unsigned PE responses in the insula are selective for pain or reflective of a more general processing of aversive events irrespective of modality. It is also unknown whether the insula can process signed PEs at all. Understanding these specific mechanisms has implications for understanding how pain is processed in the brain in both health and in chronic pain conditions. In this study, 47 participants learned associations between 2 conditioned stimuli (CS) with 4 unconditioned stimuli (US; painful heat or loud sound, of one low and one high intensity each) while undergoing functional magnetic resonance imaging (fMRI) and skin conductance response (SCR) measurements. We demonstrate that activation in the anterior insula correlated with unsigned intensity PEs, irrespective of modality, indicating an unspecific aversive surprise signal. Conversely, signed intensity PE signals were modality specific, with signed PEs following pain but not sound located in the dorsal posterior insula, an area implicated in pain intensity processing. Previous studies have identified abnormal insula function and abnormal learning as potential causes of pain chronification. Our findings link these results and suggest that a misrepresentation of learning relevant PEs in the insular cortex may serve as an underlying factor in chronic pain.
预测误差(PE)是在预期事件或感官输入与实际事件或感官输入之间存在差异时产生的。脑岛是参与疼痛处理的关键大脑区域之一,研究表明,脑岛编码了意外结果的幅度(无符号 PE)。除了发出这种一般幅度信息外,PE 还可以提供有关此偏差方向的具体信息,即事件是好于预期还是差于预期。目前尚不清楚脑岛中的无符号 PE 反应是否专门针对疼痛,或者是否反映了对痛苦事件的更一般处理,而与模态无关。也不知道脑岛是否可以处理有符号的 PE。了解这些特定的机制对于理解疼痛在健康和慢性疼痛条件下如何在大脑中处理具有重要意义。在这项研究中,47 名参与者在进行功能磁共振成像(fMRI)和皮肤电反应(SCR)测量的同时,学习了 2 个条件刺激(CS)与 4 个非条件刺激(US;每种刺激都有一个低强度和一个高强度的疼痛热或响亮的声音)之间的关联。我们证明,前脑岛的激活与无符号强度 PE 相关,而与模态无关,表明存在一种非特异性的厌恶惊喜信号。相反,有符号强度 PE 信号是模态特异性的,有符号 PE 跟随疼痛而不是声音位于背侧后脑岛,该区域与疼痛强度处理有关。先前的研究已经确定了脑岛功能异常和异常学习是疼痛慢性化的潜在原因。我们的发现将这些结果联系起来,并表明脑岛皮层中与学习相关的 PE 表示异常可能是慢性疼痛的一个潜在因素。