Mood Influences Supraspinal Pain Processing Separately from Attention

Abstract

Studies show that inducing a positive mood or diverting attention from pain decreases pain perception. Nevertheless, induction manipulations, such as viewing interesting movies or performing mathematical tasks, often influence both emotional and attentional states. Imaging studies have examined the neural basis of psychological pain modulation, but none has explicitly separated the effects of emotion and attention. Using odors to modulate mood and shift attention from pain, we previously showed that the perceptual consequences of changing mood differed from those of altering attention, with mood primarily altering pain unpleasantness and attention preferentially altering pain intensity. These findings suggest that brain circuits involved in pain modulation provoked by mood or attention are partially separable. Here we used functional magnetic resonance imaging to directly compare the neurocircuitry involved in mood-and attention-related pain modulation. We manipulated independently mood state and attention direction, using tasks involving heat pain and pleasant and unpleasant odors. Pleasant odors, independent of attentional focus, induced positive mood changes and decreased pain unpleasantness and pain-related activity within the anterior cingulate (ACC), medial thalamus, and primary and secondary somatosensory cortices. The effects of attentional state were less robust, with only the activity in anterior insular cortex (aIC) showing possible attentional modulation. Lateral inferior frontal cortex [LinfF; Brodmann's area (BA) 45/47] activity correlated with moodrelated modulation, whereas superior posterior parietal (SPP; BA7) and entorhinal activity correlated with attention-related modulation. ACC activity covaried with LinfF and periacqueductal gray activity, whereas aIC activity covaried with SPP activity. These findings suggest that separate neuromodulatory circuits underlie emotional and attentional modulation of pain.

Cerebral and spinal modulation of pain by emotions

“…In the other study, unpleasant odors, compared with pleasant ones, increased both pain perception and activations in the ACC, medial thalamus, and primary and secondary somatosensory cortices (SI/SII) (15). However, in this case, pain-related activations were confounded with activations related to odors due to the simultaneous application of odors and painful stimulation.…”

Mapping of neural activity produced by thermal pain in the healthy human spinal cord and brain stem: a functional magnetic resonance imaging study

“…For example, the entorhinal cortex of the hippocampal formation has been shown to respond differentially to identical noxious stimuli depending on whether the perceived pain intensity was enhanced by pain-relevant anxiety [25]. Additionally, Villemure and Bushnell [26] recently reported that painrelated activity within the anterior cingulate, medial thalamus and primary and secondary somatosensory cortices was correlated with mood, whereas the effects of attentional state altered activity in anterior insular cortex. The group results from the present study therefore complement these previous studies and demonstrate details of the pain matrix including the ascending pathways, the affective components of the response and the descending modulation of the response in subcortical regions.…”

Nociception and autonomic nervous system

“…In contrast, the ventrolateral column receives convergent input from both the superficial and deep dorsal horn relaying nociceptive afferent information from visceral, muscle, and C-fiber skin nociceptors as well as visceral inputs from the nucleus of the NTS and sacral spinal cord. Functional neuroimaging studies in humans indicate that PAG activation by nociceptive inputs is modulated by attention, emotion, expectation of pain and expectation-related placebo analgesia [54][55][56][57][58][59][60][61]. Experimental studies using chemical microstimulation indicate that the different columns of the PAG organize different coping strategies to pain and other stressors [62][63][64][65][66].…”