Altered pain and thermal sensation in subjects with isolated parietal and insular cortical lesions

Abstract

Studies of sensory function following cortical lesions have often included lesions which multiple cortical, white matter, and thalamic structures. We now test the hypothesis that lesions anatomically constrained to particular insular and parietal structures and their subjacent white matter are associated with different patterns of sensory loss. Sensory loss was measured by quantitative sensory testing (QST), and evaluated statistically with respect to normal values.All seven subjects with insular and/or parietal lesions demonstrated thermal hypoesthesia, although the etiology of the lesions was heterogeneous. Cold and heat hypoalgesia were only found in the subject with the most extensive parietal and insular lesion, which occurred in utero. Cold allodynia occurred clinically and by thresholds in two subjects with isolated ischemic lesions of the posterior insular/ retroinsular cortex, and by thresholds in two subjects with a lesion of parietal cortex with little or no insular involvement. Central pain occurred in the two subjects with clinical allodynia secondary to isolated lesions of the posterior insular/retroinsular cortex, which spared the anterior and posterior parietal cortex. These results suggest that nonpainful cold and heat sensations are jointly mediated by parietal and insular cortical structures so that lesions anywhere in this system may diminish sensitivity. In contrast, thermal pain is more robust requiring larger cortical lesions of these same structures to produce hypoalgesia. In addition, cold allodynia can result from restricted lesions that also produce thermal hypoesthesia, but not from all such lesions.

Neurophysiology of Skin Thermal Sensations

“…However, recent neuroanatomical work in primate models (58) along with neuroimaging results from human studies (61,62,157), have repeatedly challenged this view (67). Strong evidence has been indeed provided not only for the fact that other cortical areas than the somatosensory one could be involved in thermal processing, but that in fact these areas could play a more specific role in sub-serving temperature (as well as pain) (263) sensations in humans (19,62,237,296). Amongst these areas, the dorsal margin of the posterior insular cortex has been proposed as the specific area for the cortical processing of both the discriminative (157) and affective (62,251) components of thermal sensations in humans.…”

“…cold) (19) thermo-anesthesia in humans. For example, in a recent quantitative sensory analysis, warm and cold hypoesthesia was consistently recorded in patients with constrained cortical lesions located in the insular and parietal cortices (296). Interestingly, lesions of the human insular cortex not only induce thermosensory deficits, but also, these are very often accompanied by the development of central pain (19,296).…”

Deconstructing Central Pain with Psychophysical and Neuroimaging Studies

“…This has been demonstrated for patients with lesions of the spinal cord (Ducreux et al, 2006;Finnerup et al, 2003), and brain Garcia-Larrea et al, 2010). In the case of cortical lesions, the results of a recent study demonstrate warm and cold hypoesthesia based on QST thresholds in all subjects with lesions of parietal or insular cortex or both (Veldhuijzen et al, 2009). The largest degree of thermal hypoesthesia by threshold measures was found in the subject with the largest lesion, which involved extensive parietal and insular lobar lesions (see also (Greenspan et al, 1999).…”

“…A recent study has suggested that CPSP occurred only in individuals with lesions including posterior insula/retroinsula, which spare the anterior and posterior parietal cortex (Veldhuijzen et al, 2009). Evidence from neuroimaging studies suggests that the parietal lobe is involved in the mechanism of CPSP and CPSP-associated allodynia in subjects with strokes of the lateral medulla (Wallenberg syndrome) (Peyron et al, 1998), and the thalamic nucleus Vc which projects to the parietal cortex .…”

“…The expression of cold allodynia is variable, which suggests that there is more than one mechanism for cold allodynia in different patients. In our recent study of seven patients with isolated parietal and/or insular lesions, 4/7 patients had cold allodynia based on thresholds, but only two of these had central pain and clinical cold hyperalgesia based on increased ratings of a painful cold waterbath stimulus (Veldhuijzen et al, 2009). Overall, these results suggest that posterior insular/retroinsular lesions in isolation can lead to cold allodynia as assessed by clinical, threshold and suprathreshold measures.…”