Neural substrates underlying evaluation of pain in actions depicted in words

Abstract

Previous research has shown that evaluation of pain shown in pictures is mediated by a cortical circuit consisting of the primary and secondary somatosensory cortex (SI and SII), the anterior cingulate cortex (ACC), and the insula. SI and SII subserve the sensory-discriminative component of pain processing whereas ACC and the insula mediate the affective-motivational aspect of pain processing. The current work investigated the neural correlates of evaluation of pain depicted in words. Subjects were scanned using functional magnetic resonance imaging (fMRI) while reading words or phrases depicting painful or neutral actions. Subjects were asked to rate pain intensity of the painful actions depicted in words or counting the number of Chinese characters in the words. Relative to the counting task, rating pain intensity induced activations in SII, the insula, the right middle frontal gyrus, the left superior temporal sulcus and the left middle occipital gyrus. Our results suggest that both the sensory-discriminative and affective-motivational components of the pain matrix are engaged in the processing of pain depicted in words.

Introduction

It is well documented that pain processing is mediated by a neural network consisting of both cortical and subcortical structures. The cortical structures of the pain matrix includes the primary and secondary somatosensory cortex (SI and SII), the anterior cingulate cortex (ACC), the insula and prefrontal regions, whereas the subcortical components of the pain matrix includes the thalamus, amygdala and hippocampus, etc. [1], [2]. Nociceptive specific neurons in SI and SII respond only to noxious stimuli [3], [4], [5] and their receptive fields are organized in a somatotopic pattern (particularly in the post-central gurys) [6]. Neuroimaging studies also showed evidence that painful stimulation induced increased hemodynamic responses in SI and SII [7] or resulted in positive covariation between the activity in SI and other brain regions that are known to be involved in pain processing [8]. These findings suggest that SI and SII play an important role in the sensory-discriminative component of pain processing. Recent neuroimaging studies show that while the activity of ACC and the insula can be increased by noxious stimuli [9], [10], illusions evoked by non-noxious stimuli [11] and perception of others in pain [12], [13], [14], [15] also induce activation in ACC and the insula. In addition, the magnitude of ACC activity is correlated with subjective pain-related unpleasantness [9]. These results indicate that ACC and the insula subserve the affective-motivational component of pain processing.

Most of the previous studies of pain processing employed noxious stimuli such as thermal or mechanical stimulation. However, people often encounter ‘painful’ information when noxious stimuli are absent. For example, words or phrases such as “prick” and “hit by a car” are used in novels or newspapers to describe painful situations. To date, we know little about whether the same brain circuits underlying pain processing can also be activated by pain evaluation depicted in words. In particular, it is unclear if both the sensory-discriminative and the affective-motivational components of the pain matrix are involved in evaluation of pain depicted in words. Osaka et al. found that ACC can be activated when subjects were asked to form unpleasant mental images of affective pain corresponding to onomatopoeia words suggestive of subjective pain presented auditorily [16]. The current study extended the previous work by assessing whether evaluation of pain described in words or short phrases presented visually induces activation of the pain matrix. One possibility is that reading words or phrases depicting painful actions is similar to watching painful pictures in generating empathic responses mediated by the pain matrix. Alternatively, words or phrases cannot produce painful situations as vivid as those illustrated in pictures and, thus, cannot activate the neural circuit underlying empathy for pain. We addressed these issues by recording heomodynamic responses from human adults using functional magnetic resonance (fMRI). Brain activity linked to rating pain intensity of actions described in Chinese words or phrases presented visually was contrasted with reading words or phrases describing neutral actions so as to identify whether the somatosensory cortex and other brain areas such as ACC and insula are involved in evaluation of pain depicted in words. We also compared the tasks of counting the number of Chinese characters in painful and neutral words to assess the necessity of the rating task in activation of the pain matrix.