Chantal Villemure

Cognitive modulation of pain: how do attention and emotion influence pain processing?

There have been anecdotal accounts for centuries of people apparently experiencing little or no pain in situations that most of us would find excruciating. Yet, western medicine has given little credence to a patient’s ability to modify pain. Instead, we focus on the pharmacological control of pain. For this reason, the vast majority of research on pain control has concentrated on peripheral and spinal cord mechanisms of opioid and anti-inflammatory analgesic therapy. Nevertheless, researchers are beginning to recognize that a variety of pain modulatory mechanisms exist in the nervous system, and these modulatory systems can be accessed either pharmacologically or through contextual and/or cognitive manipulation (Fields, 2000). Variables such as attentional state, emotional context, hypnotic suggestions, attitudes, expectations or anesthesia-induced changes in consciousness now have been shown to alter both pain perception and forebrain pain transmission in humans. These techniques, at times, preferentially alter sensory and/or affective aspects of pain perception, and the associated modulation of pain-evoked neural activity occurs in limbic and/or sensory brain regions, suggesting multiple endogenous pain-modulatory systems. This paper compares the modulatory influences of two principal cognitive variables, attention and emotion, on pain perception and addresses possible neural mechanisms underlying each of these influences.

Effects of odors on pain perception: deciphering the roles of emotion and attention

&NA; Emotions have been shown to alter pain perception, but the underlying mechanism is unclear since emotions also affect attention, which itself changes nociceptive transmission. We manipulated independently direction of attention and emotional state, using tasks involving heat pain and pleasant and unpleasant odors. Shifts in attention between the thermal and olfactory modalities did not alter mood or anxiety. Yet, when subjects focused attention on the pain, they perceived it as clearly more intense and somewhat more unpleasant than when they attended to the odor. In contrast, odor valence altered mood, anxiety level, and pain unpleasantness, but did not change the perception of pain intensity. Pain unpleasantness ratings correlated with mood, but not with odor valence, suggesting that emotional changes underlie the selective modulation of pain affect. These results show that emotion and attention differentially alter pain perception and thus invoke at least partially separable neural modulatory circuits.

The effects of the steroid androstadienone and pleasant odorants on the mood and pain perception of men and women.

Background and purpose. We previously found that for both men and women odors influence mood, which in turn influences pain unpleasantness perception. Others showed that the steroid androstadienone modulates mood differently in men and women, improving mood in women and worsening it or leaving it unchanged in men. Based on its dissociable effect on mood, we hypothesized that women exposed to androstadienone would report lower pain unpleasantness than when exposed to the vehicle, while men would show no change or the reverse pattern. Because of the expected beneficial effect of pleasant odors on mood in both men and women, all subjects should report lower pain unpleasantness when exposed to the pleasant odor compared to the unscented air.

Supraspinal Pain Processing: Distinct Roles of Emotion and Attention

Attentional and emotional states alter the way we perceive pain. Recent findings suggest that the mechanisms underlying these two forms of pain modulation are at least partially separable. This concept is supported by the observation that attention and emotions differentially alter the sensory and affective dimensions of pain perception and apparently implicate different brain circuits. In this review, we will examine those recent findings within the broader cognitive neuroscience conceptualization of human attention and emotion and the corresponding functional neuroanatomy.

Imaging pain in the brain: The role of the cerebral cortex in pain perception and modulation.

SUMMARY Objectives: This review examines data from human neuroimaging studies, in an effort to better understand the neural basis of the conscious appreciation of pain. Included is evidence from experimental studies of normal pain processing and pain modulation by psychological state. Also reviewed is evidence from studies of patients with chronic pain syndromes, such as neuropathic pain, central pain, and fibromyalgia, that may involve aberrant forebrain processing of nociceptive information. Findings: Both positron emission tomography and functional magnetic resonance imaging studies of experimental pain in normal subjects reveal a complex network of neural activity in the cerebral cortex that likely underlies the conscious appreciation of pain. The totality of sensory and emotional experience associated with pain varies among individuals and circumstances, and these dissimilarities are reflected in variations in patterns of neural activation observed among studies. However, striking commonalities are observed among studies, including the activation of sensory regions, such as primary and secondary somato-sensory cortices and limbic areas such as anterior cingulate cortex and insular cortex. Studies of cognitive modulation of pain show that the degree of activation of these regions is dependent on cognitive factors, such as attentional state, that alter our perception of pain. Finally, imaging studies of patients with chronic pain states often reveal abnormalities of pain processing that result in the “cortical pain network” being activated by normally nonpainful stimuli, thus providing a neural basis for perceptual phenomena such as allodynia and hyperalgesia. Conclusions: There is a common network of cortical and subcortical structures that subserves the pain experience. Whether this network is activated by tissue-damaging stimuli in a “normal” situation, or by non-noxious stimuli such as a light brush or cool breeze on the skin in pathological conditions, the final experience associated with its activation is pain. Finally, activity in this network can be modulated by cognitive state, as well as by pharmacological treatments, leading to an alteration of the pain experience.

Unpleasant odors increase pain processing in a patient with neuropathic pain: Psychophysical and fMRI investigation

Abstract A 49‐year old man with neuropathic pain in his right elbow, wrist and digits III–V of his hand reported that certain odors increased his pain by superimposing an electric shock‐like pain to his already existing pain. Psychophysical testing revealed that the best predictor of pain exacerbation was odor unpleasantness. Functional magnetic resonance imaging (fMRI) showed increased activation following an unpleasant odor in pain related areas, including the thalamus, amygdala, insular and anterior cingulate cortices, with similar trends in primary somatosensory cortex hand/arm area. The increased pain and associated neural activations in response to unpleasant odors may be related to the phenomenon of synesthesia, to a rewiring of olfactory pathways onto pain pathways mimicking synesthesia or, to activation of the sympathetic nervous system.

The Ventral Striatum is Implicated in the Analgesic Effect of Mood Changes

BACKGROUND The ventral striatum, particularly the nucleus accumbens, is commonly associated with the processing of reward and positive stimuli, positive affect as well as antinociceptive processes. OBJECTIVES The present study examined whether the ventral striatum is implicated in analgesia resulting from positive mood change induced by pleasant odours. METHODS Functional magnetic resonance imaging studies were conducted in healthy individuals receiving painful heat stimuli in the presence of pleasant or unpleasant odours, which were used to induce positive and negative mood states. Ventral striatum activity was examined in the two mood states. RESULTS For most subjects, pleasant odours improved mood and reduced pain unpleasantness perception relative to unpleasant odours. In the pleasant odour condition, the maximum activation of both the left and right ventral striatum was positively correlated with the amount of pain reduction. Furthermore, the left and right ventral striatum activations positively covaried with one another, and the right ventral striatum activation positively correlated with that in the periaqueductal grey matter. Both ventral striatum activations negatively covaried with the activation of the right mediodorsal thalamus, left dorsal anterior cingulate cortex, left medial prefrontal cortex and right ventrolateral prefrontal cortex. CONCLUSIONS Because both the mediodorsal thalamus and anterior cingulate are involved in pain affect perception, and activation within the prefrontal areas and periaqueductal grey matter were previously shown to correlate with mood-related pain modulation, it is concluded that the ventral striatum is likely implicated in the analgesic effect of positive mood changes induced by pleasant odours on pain unpleasantness.