Cerebral and spinal modulation of pain by emotions - PubMed (original) (raw)

Clinical Trial

. 2009 Dec 8;106(49):20900-5.

doi: 10.1073/pnas.0904706106. Epub 2009 Nov 19.

Affiliations

Clinical Trial

Cerebral and spinal modulation of pain by emotions

Mathieu Roy et al. Proc Natl Acad Sci U S A. 2009.

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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Experimental paradigm and brain responses to painful shocks and pictures. (A) Each trial consists of a block of five 6-s pictures (neutral, pleasant, or unpleasant), within which two painful electrical stimulations are delivered 2,700 ms after the onset of the 2nd and 4th pictures. At the end of the trial, participants were asked to rate the mean pain elicited by the two painful stimulation on a VAS. (B) Electrical stimulations were delivered over the right sural nerve (ankle) and RIII reflexes were extracted from the EMG of the biceps femoris in a window of 90–180 ms after the onset of the electrical stimulation. (C) A mixed block/event-related model was used to analyze the data. Pictures were modeled as blocks and electrical stimulations as events. (D) Electrical stimulations elicited activations in the thalamus (Thal), hypothalamus (Hyp), SI/SII, ACC, insula (Ins), precentral gyrus (PCG), SMA, OFC, and cerebellum (Cb). Pictures elicited activation in visual areas such as the inferior occipital gyrus (IOG) and fusiform gyrus (FFG) (see

Table S1

).

Fig. 2.

Fig. 2.

Modulation of pain-related responses by the emotional conditions. (A) Effects of the experimental condition on pain ratings (Upper). Effects of the experimental condition on the standardised R-III reflex amplitudes (Lower). *, P < 0.05. (B) Regions where shock-related activity was higher during the viewing of unpleasant compared with pleasant pictures included the PCL, right Ins, and bilateral PHG. (C) Regions where the amplitude of the modulation of brain responses between unpleasant and pleasant pictures correlated with the corresponding modulation in RIII reflex or pain ratings. (Left) Correlations with RIII reflex modulation included the left medial Thal, left pons, bilateral amygdalae (Amy), SgCC, VMPFC and MPFC, and Cb. (Right) Correlations with pain modulation (pain ratings) included the right Ins and bilateral lingual gyri (LG). Activation maps are thresholded at P < 0.005 for display purposes (see

Tables S2 and S3

).

Fig. 3.

Fig. 3.

Results of the PPI analyses. (A) The psychological variable for the interaction is the contrast between the electrical stimulations presented during unpleasant vs. pleasant pictures. (B) Right OFC, SgCC, and cuneus (Cun) exhibited higher connectivity with the right insula for the electrical stimulations presented during the viewing of unpleasant vs. pleasant pictures (Left). Left DLPFC, FFG, and PHG, left SMA, left Thal, and RM showed higher connectivity with the PCL for the electrical stimulations presented during the viewing of unpleasant vs. pleasant pictures (Right). (C) The right Ins and the PCL, where activation to electrical stimulations were shown to be higher during unpleasant than pleasant pictures, served as the physiological variables (“seeds”) for the PPIs. Activation maps were thresholded at P < 0.005 for display purposes (see

Table S5

).

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