Cerebral and spinal modulation of pain by emotions

Abstract

Emotions have powerful effects on pain perception. However, the brain mechanisms underlying these effects remain largely unknown. In this study, we combined functional cerebral imaging with psychophysiological methods to explore the neural mechanisms involved in the emotional modulation of spinal nociceptive responses (RIII-reflex) and pain perception in healthy participants. Emotions induced by pleasant or unpleasant pictures modulated the responses to painful electrical stimulations in the right insula, paracentral lobule, parahippocampal gyrus, thalamus, and amygdala. Right insula activation covaried with the modulation of pain perception, consistent with a key role of this structure in the integration of pain signals with the ongoing emotion. In contrast, activity in the thalamus, amygdala, and several prefrontal areas was associated with the modulation of spinal reflex responses. Last, connectivity analyses suggested an involvement of prefrontal, parahippocampal, and brainstem structures in the cerebral and cerebrospinal modulation of pain by emotions. This multiplicity of mechanisms underlying the emotional modulation of pain is reflective of the strong interrelations between pain and emotions, and emphasizes the powerful effects that emotions can have on pain. Descending pain-modulatory pathways originate from various cerebral structures involved in emotions (6-8) and sensorimotor functions (9). These regions are thought to affect spinal nociception through their projections to several brainstem structures, including the periaqueductal gray matter (PAG), rostroventral medulla (RVM), dorsolateral pontine tegmentum (DLPT), and nucleus cuneiformis (NCF) (10). All of these structures are thus potential cerebral sources of the descending modulation of pain by emotions. In turn, the modulation of spinal activity is expected to affect the transmission of nociceptive signals and the response of their target brain regions through the multiple ascending pathways. However, the important interconnectivity between emotional brain networks and areas implicated in the affective dimension of pain suggests that additional supraspinal mechanisms might also contribute to the emotional modulation of pain experiences. Among the potential cortical candidates, the anterior cingulate cortex (ACC) (11) and the insula (12) are well positioned to contribute to the emotional modulation of pain.Whereas the ACC appears to be involved in the motoric and motivational aspects of pain and emotions, the insula is thought to generate subjective interoceptive feelings as a result of the gradual posterior-to-anterior integration of primary interoceptive information with contextual emotional and cognitive information (12).The cerebral correlates of the emotional modulation of pain perception have been explored in two brain imaging studies. In one study, pain-related activation in the entorhinal cortex was increased by expectation-induced anticipatory anxiety of a highly painful stimulation (13). Also, the increased activation in the entorhinal...

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