Vicarious Responses to Social Touch in Posterior Insular Cortex Are Tuned to Pleasant Caressing Speeds

Vicarious Responses to Social Touch in Posterior Insular Cortex Are Tuned to Pleasant Caressing Speeds
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DOI:
10.1523/jneurosci.0397-11.2011
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发表时间:
2011-06-29
影响因子:
5.3
通讯作者:
Olausson, Hakan
Olausson, Hakan
中科院分区:
医学1区
文献类型:
--
作者:
Morrison, India;Bjornsdotter, Malin;Olausson, Hakan

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背景。情感触摸对包括人类在内的社会性哺乳动物具有重要意义。轻柔的、动态的触觉发生在社交互动中,它被一条独特的神经通路优先编码,该通路涉及触觉C (CT)传入神经,这是一种只存在于多毛皮肤中的无髓传入神经。当以类似于3厘米/秒的愉快的爱抚速度抚摸皮肤时,CT传入神经会增加放电,其放电频率与爱抚的主观享乐体验相关。在人类中,脑岛后部是CT传入事件的皮质靶点。由于情感触摸的潜在社会关联延伸到他人的触摸互动,我们假设来自后岛叶皮层CT传入的信息为观察到的爱抚提供了编码的基础。在两个实验中,我们利用了CT传入事件在功能上独特的抚摸速度调节曲线,证明激发CT放电的最佳速度(3厘米/秒)也比非最佳速度(30厘米/秒)在脑岛后部产生更高的BOLD反应。当参与者观看别人的手臂被以ct最佳和非最佳速度抚摸的视频时,后脑岛显示出与直接触摸相似的反应。此外,该区域对社交互动的反应是特定的,对非社交动态触摸视频没有显示出与ct相关的调制。这些发现为CT信号与后岛叶皮层处理之间的功能关系提供了直接证据。这种对脑岛ct最佳信号的选择性调谐可能允许识别仅仅观察到的爱抚的享乐相关性。
Background. Affective touch carries strong significance for social mammals, including humans. Gentle, dynamic touch of a kind that occurs during social interactions is preferentially encoded by a distinct neural pathway involving tactile C (CT) afferents, a type of unmyelinated afferent nerve found exclusively in hairy skin. CT afferents increase firing when the skin is stroked at a pleasant, caress-like speed of similar to 3 cm/s, and their discharge frequency correlates with the subjective hedonic experience of the caress. In humans, the posterior insula is a cortical target for CT afferents. Since the potential social relevance of affective touch extends to the touch interactions of others, we postulated that information from CT afferents in posterior insular cortex provides a basis for encoding observed caresses.Results. In two experiments, we exploited CT afferents' functionally unique tuning curve for stroking speed, demonstrating that a speed optimal for eliciting CT discharge (3 cm/s) also gives rise to higher BOLD responses in posterior insula than a nonoptimal speed (30 cm/s). When participants viewed videos of others' arms being stroked at CT-optimal versus -nonoptimal speeds, the posterior insula showed a similar response as to directly felt touch. Further, this region's response was specific for social interactions, showing no CT-related modulation for nonsocial dynamic-touch videos.Conclusions. These findings provide direct evidence for a functional relationship between CT signaling and processing in posterior insular cortex. Such selective tuning for CT-optimal signals in insula may allow recognition of the hedonic relevance of a merely observed caress.