Abstract

By definition, patients with unresponsive wakefulness syndrome (UWS) do not experience pain, but it is still not completely understood how far their brain can process noxious stimuli. The few positron emission tomography studies that have examined pain processing did not yield a clear and consistent result. We performed an functional magnetic resonance imaging scan in 30 UWS patients of nontraumatic etiology and 15 age- and sex-matched healthy control participants (HC). In a block design, noxious electrical stimuli were presented at the patients' left index finger, alternating with a resting baseline condition. Sixteen of the UWS patients (53%) showed neural activation in at least one subsystem of the pain-processing network. More specifically, 15 UWS patients (50%) showed responses in the sensory-discriminative pain network, 30% in the affective pain network. The data indicate that some patients completely fulfilling the clinical UWS criteria have the neural substrates of noxious stimulation processing, which resemble that in control individuals. We therefore suppose that at least some of these patients can experience pain.

Highlights

  • Pain is defined as an unpleasant sensory and emotional experience, associated with real or potential tissue damage (Merskey and Bogduk 1994) and including both physical and affective aspects (Kupers et al 2005).In individuals with preserved consciousness, both positron emission tomography (PET) and functional magnetic resonance imaging reveal a well-formed network of interrelated brain regions responding to pain stimuli, the so-called pain matrix

  • The cerebellum does not belong to the so-called pain matrix, it is known that it plays a role in processing aversive stimuli including pain (Moulton et al 2011)

  • No significant group difference was found in the cerebellum (v2 = 0.42, P = 0.52) and in the anterior cingulate cortex (ACC) (v2 = 2.95, P = 0.172). This is the first study investigating the individual brain activations elicited by noxious stimuli in a large homogenous sample of unresponsive wakefulness syndrome (UWS) patients using functional magnetic resonance imaging (fMRI)

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Summary

Introduction

Pain is defined as an unpleasant sensory and emotional experience, associated with real or potential tissue damage (Merskey and Bogduk 1994) and including both physical (i.e., nociception which means the detection of painproducing stimuli by primary sensory neurons) and affective aspects (i.e. suffering) (Kupers et al 2005).In individuals with preserved consciousness, both positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) reveal a well-formed network of interrelated brain regions responding to pain stimuli, the so-called pain matrix. Pain is defined as an unpleasant sensory and emotional experience, associated with real or potential tissue damage (Merskey and Bogduk 1994) and including both physical (i.e., nociception which means the detection of painproducing stimuli by primary sensory neurons) and affective aspects (i.e. suffering) (Kupers et al 2005). The pain matrix entails two main subsystems (Brooks and Tracey 2005): the lateral neuronal network that encodes sensory-discriminative information consists of the primary (S1) and the secondary somatosensory (S2) cortex, the lateral thalamus, and the posterior insula (Mutschler et al 2011). The medial network that encodes affective-cognitive information consists of the anterior insula, the anterior cingulate cortex (ACC), and the prefrontal cortex (Wiech et al 2001; Medford and Critchley 2010). It can be counted to the sensory-discriminative part of the pain-

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