© 2008 American Thoracic Society doi: 10.1164/rccm.200802-298ED
Dyspnea and EmotionWhat Can We Learn from Functional Brain Imaging?
Hôpital Européen Georges Pompidou It is commonly accepted that emotion plays an essential role in the subjective experience of dyspnea. However, the involvement of emotion in the central processing of dyspnea is both complex and manifold (1). Emotion may induce dyspnea, either alone but generally together with physical stimuli, and may interfere with virtually all of the different stages of dyspnea processing from initial crude sensory perception to the final complex subjective experience. On the basis of clinical observations, as well as on the striking similarities between dyspnea and pain, it has been hypothesized that dyspnea might encompass at least two distinct, albeit interacting, dimensions (i.e., sensory and affective/cognitive), as has been demonstrated for pain (2, 3). As suggested by a validated model of pain perception (3), the affective dimension of dyspnea presumably further includes an immediate emotional reaction (i.e., dyspnea-related unpleasantness, possibly associated with an autonomic response) and a secondary, more sophisticated affective reaction to dyspnea (corresponding to dyspnea suffering) involving higher order cognitive functions, such as evaluation, memory, and mental representation, which subsequently leads to changes in dyspnea-related behavior, including coping. The secondary multistage reaction to dyspnea is, as suggested by Comroe in 1966, part of this sensation (4), and is presently included in the definition of dyspnea (5). Wilson and Jones were the first to demonstrate that intensity and dyspnea-related distress (the latter presumably corresponding to both the immediate and secondary affective reaction described for pain [3]) are indeed two different and distinguishable components of dyspnea that can be assessed and vary independently (6). In a given subject, although the intensities of both components are highly related, there is a large interindividual variation in the ratio of dyspnea-related distress and intensity. This result provided new insights into dyspnea processing, and may be highly relevant for our understanding of dyspnea. Indeed, intersubject differences in the intensity/distress relationship further increase the complexity of the relationship between the intensity of the supposed underlying stimulus of dyspnea and the final subjective experience of this sensation. It is conceivable that, in addition to abnormally low or high global dyspnea intensity score, diminished or increased perception of dyspnea may be related to an impaired and exaggerated perception of dyspnea-related unpleasantness, respectively. Finally, because it involves suffering, it is likely that the affective component of dyspnea is a more relevant determinant of disease-related behavior (i.e., seeking medical help or compliance with treatment) than the perception of dyspnea intensity. More recently, it has been further demonstrated that for dyspnea, as largely documented for pain (2, 3), the sensory and affective components can be manipulated independently (7, 8), which may have considerable relevance regarding therapeutic interventions. An important challenge in dyspnea research was to identify the cerebral structures involved in central integration of sensory and emotional aspects and their interactions, and more specifically, to determine whether, as previously documented for pain (9), there is some partial functional segregation of the corresponding brain areas. In our first imaging study (10), we identified an activation area in the right posterior cingulate cortex that was associated with perceived intensity of dyspnea but not related to that of the underlying physical stimulus and thus possibly involved in the modulation of dyspnea intensity by affective/cognitive factors. In this issue of the Journal (pp. 1026–1032), von Leupoldt and colleagues (11) determined brain activation associated with the affective component of dyspnea. Using an elegant design that allowed for independent manipulation of negative emotion by presenting affectively charged pictures during the sessions of acute short-term, load-induced dyspnea, the authors showed that dyspnea unpleasantness was associated with a characteristic activation pattern involving the right anterior insula and the right amygdala. Although it remains to be verified that the unpleasantness attributed to dyspnea is actually and entirely related to dyspnea per se rather than to the negative emotions elicited by the unpleasant pictures, the results of this study provide important new insights into the central processing of interactions between negative emotion and dyspnea perception. However, neither of the two corresponding brain structures detected by von Leupoldt and colleagues (11), the anterior insula and the amygdala, nor the posterior cingulate gyrus identified by our study (10) is specifically devoted to dyspnea processing. Indeed, as discussed in both studies (10, 11), activity in these brain structures has been identified for a host of different, mostly unpleasant sensory experiences, especially pain (12–14), and cognitive functions (13, 14), but also, especially for the insula, autonomic arousal (15). These findings suggest that the complex interactions between emotion and sensory perception involve common networks, including a limited number of crucial integration areas for sensory-motor and affective/cognitive information, like the anterior insula and the cingulate cortex. These results also indicate that dyspnea processing shares several neural networks with those for other, similarly complex and predominantly unpleasant sensations, such as pain, hunger, thirst, and disgust. It cannot be excluded that future imaging techniques with higher spatial resolution will unravel some subtle functional segregation within these consistently activated areas in dyspnea perception, possibly in relation with structural histologic differences (16). It is noteworthy that, in the study of von Leupoldt and colleagues (11), the activation area associated with dyspnea unpleasantness in the insula is very close to one of the three activation peaks included in a larger activation cluster corresponding to the comparison of dyspnea with the unloaded control condition. The challenge of future neuroimaging research of dyspnea will be to determine the spatial and temporal characteristics of the complex interactions between the different components of the large set of brain structures involved in dyspnea processing, the "dyspnea neuromatrix," which ultimately may determine the specificity of the complex sensation of dyspnea. FOOTNOTES Conflict of Interest Statement: The author has no financial relationship with a commercial entity that has an interest in the subject of this manuscript. REFERENCES
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