The contribution of cutaneous thermal signals to bodily self-awareness

Abstract

Thermosensory signals may contribute to the sense of body ownership, but their role remains highly debated. We test this assumption within the framework of pathological body ownership, hypothesising that skin temperature and thermoception differ between right-hemisphere stroke patients with and without Disturbed Sensation of Ownership (DSO) for the contralesional plegic upper limb. Patients with DSO exhibit lower basal hand temperatures bilaterally and impaired perception of cold and warm stimuli. Lesion mapping reveals associations in the right Rolandic Operculum and Insula, with these regions linked to lower skin temperature located posterior to those associated with thermoception deficits. Disconnections in bilateral parietal regions are associated with lower hand temperature, while disconnections in a right-lateralized thalamus-parietal hub correlate with thermoception deficits. We discuss the theoretical implications of these findings in the context of the ongoing debate on the role of homeostatic signals in shaping a coherent sense of body ownership.

Fig. 1. Skin temperature and thermoception results.

In the left panel, the grey-shaded boxplots display the basal skin temperature (measured in Celsius) distribution across the three different groups of patients, separately by sides (left in light green vs. right in dark green). The central line indicates the median value (50th percentile), while the bounds of the box represent the 25th (lower bound) and 75th percentiles (upper bound), i.e., interquartile range (IQR). The whiskers extend to the minimum and maximum values within 1.5 times the IQR. Jittered points represent the individual data points, while the estimated marginal means for each group and side are shown as larger bold dots (circles for the left side, triangles for the right side), with error bars representing 95% confidence intervals. Solid lines indicate the left side, and dotted lines indicate the right side. To investigate whether the baseline skin temperature of the limb differed between the groups based on the subjective experience of disownership, we performed a General Linear Model with Group (HP+ DSO+ (n = 9), HP+ DSO− (n = 10), HP− DSO− (n = 21)) and Side (left, right) as fixed factors. The temperature was modelled as the dependent variable. Sex and proprioception were included as covariates in the final model. For the hands’ temperature, results showed a main effect of Group (F_(2,79) = 6.126, p = 0.003; η²_p = 0.145). Post hoc Bonferroni-corrected comparisons indicated a difference between HP+ DSO+ and HP+ DSO− (p = 0.007) and between HP+ DSO+ and HP− DSO− (p = 0.005), and no difference between HP+ DSO− and HP− DSO− (p > 0.05). There was no effect of Side (F_(1,79) = 0.583, p = 0.45; η²_p = 0.008) nor a Group by Side interaction (F_(2,79) = 0.093, p = 0.911; η²_p = 0.003). To address the unbalanced group sample size and verify the robustness of the results, non-parametric bootstrap resampling based on distribution’s quintiles with 5000 replicates stratified by group was employed to estimate 95% bootstrap confidence intervals for post hoc pairwise comparisons. Results showed statistically significant differences between HP+ DSO+ and HP+ DSO− (estimate = 1.73, 95% CI [0.71;2.76], p_adj = 0.001) and between HP+ DSO+ and HP− DSO− (estimate = 2.162, 95% CI [0.99;3.40], p_adj = 0.004), and no difference between HP+ DSO− and HP− DSO− (estimate = 0.43, 95% CI [−0.56;1.38], p_adj > 0.05). The right panel shows the average number of stimuli detected in the thermoception task by the three groups of patients, separately by left (light green) and right (dark green) hand. The bold dots represent the estimated marginal means for each group and side, with error bars denoting 95% confidence intervals. Solid lines indicate the left side, and dotted lines indicate the right side. To investigate whether DSO was associated with reduced hand thermoceptive ability, we ran a Generalized Linear Model with Group (HP+ DSO+ (n = 8), HP+ DSO− (n = 7), HP− DSO− (n = 19)), Side (left, right), and Stimulus type (warm, cold) as fixed factors. The thermoception score (ranging from 0 to 3) was modelled as the dependent variable. We adopted a Poisson distribution with a square root link function to optimise the model stability. The results showed a main effect of Group (x²₍₂₎ = 15.993, p < 0.001), indicating that HP+ DSO+ performed worse than the other two groups. There was a main effect of Side (x²₍₁₎ = 21.789, p < 0.001), with an overall lower temperature detection on the left hand. We also found a Group by Side interaction (x²₍₂₎ = 30.880, p < 0.001). Bonferroni-corrected post hoc comparisons showed that HP+ DSO+ were less accurate in perceiving thermal stimuli on the left hand compared to HP+ DSO− (p = 0.008) and HP− DSO− (p < 0.001). Similarly, HP+ DSO− showed less accuracy on the left hand than HP− DSO− (p = 0.009). Furthermore, both HP+ DSO+ (p < 0.001) and HP+ DSO− (p = 0.001) showed a left-right side difference in thermoception, performing worse with the left hand as compared with the right hand, while HP− DSO− did not (p > 0.05). The main effect of Stimulus (cold vs. warm stimuli) was not significant (x²₍₁₎ = 2.728, p = 0.099), as well as the Group by Stimulus (x²₍₂₎ = 0.388, p = 0.824), Side by Stimulus (x²₍₁₎ = 0.121, p = 0.727), and Group by Side by Stimulus (x²₍₂₎ = 0.111, p = 0.946) interactions. Extrapersonal USN was the only covariate that was significant (p = 0.005). To address the unbalanced group sample size and verify the robustness of the results, non-parametric bootstrap resampling based on distribution’s quintiles with 5000 replicates stratified by group was employed to estimate 95% bootstrap confidence intervals for planned post hoc pairwise comparisons. Results from bootstrap resampling showed statistically significant differences for thermoception on the left hand between HP+ DSO+ and HP+ DSO− (estimate = 0.612, 95% CI [0.178;0.921], p_adj = 0.04), HP+ DSO− and HP− DSO− (estimate = 0.522, 95% CI [0.222;0.919], p_adj = 0.008), and between HP+ DSO+ and HP− DSO− (estimate = 1.133, 95% CI [0.835;1.368], p_adj < 0.001). All analyses were two-sided. HP hemiplegia, present (+) or absent (−), DSO Disturbed Sensation of Ownership, present (+) or absent (−), HP+ DSO+ patients with hemiplegia and disturbances in the sense of body ownership, HP+ DSO− patients with hemiplegia and without disturbances in the sense of body ownership, HP− DSO− patients without hemiplegia or disturbances in the sense of body ownership, USN unilateral spatial neglect. Source data are provided as a Source Data file.

Fig. 2. Voxel-based lesion-symptom mapping (VLSM) results.

The upper panel shows the brain regions whose lesions were associated with lower basal left and right hand skin temperature in all patients. We ran a t-test at each voxel to relate the voxel status (lesioned or spared) and a continuous temperature score, which was computed by averaging the left-right hand raw temperature, adjusted by sex and proprioception. We explored lesion-symptom associations including the whole sample of 40 patients to maximise the statistical power. The lower panel shows the brain region whose lesion was associated with a reduced ability to discriminate both cold and warm stimuli. Using a voxelwise approach, we ran a t-test at each voxel to relate the voxel status (lesioned or spared) and a continuous thermoception score. This score was obtained by averaging the number of detected stimuli in the warm and cold conditions for the left hand, mirroring the effect found in the behavioural analyses. We explored lesion-symptom associations including the whole sample of 34 patients to maximise the statistical power. In both cases, we adopted a one-tailed 0.05 alpha threshold with 10,000 permutations. The permutation-based correction was applied to maximise power while maintaining control of the FWER. The statistical tests performed are one-tailed; that is, brain injury leads to impaired behavioural performance. Z-coordinates of each axial slice are given. In each axial slice, the right hemisphere is on the right side. The level of the axial slices has been marked by a red line on the sagittal view of the brain. The colour scale illustrates the corresponding Z values.

Fig. 3. Skin temperature–connectome-based lesion-symptom mapping (CLSM) results.

We analysed the patients’ dysconnectivity matrices through a mass-univariate analysis to identify associations between parcel-to-parcel disconnections and skin temperature. Maximum statistic permutation (n = 10,000) was employed on permuted behavioural data and the original disconnection data to assess the distribution of maximum statistics under the null hypothesis. To adopt a more conservative approach, we applied a one-sided corrected threshold for statistical significance at p < 0.01 by identifying the 99th percentile of permutation-derived maximum statistics. Results are visualised with the BrainNet Viewer (http://www.nitrc.org/projects/bnv/). The image presents the disconnections significantly associated with lower left and right hand skin temperature. Dots indicate regions at the endpoints of significant disconnections.

Fig. 4. Thermoception–connectome-based lesion-symptom mapping (CLSM) results.

We analysed the patients’ dysconnectivity matrices through a mass-univariate analysis to identify associations between parcel-to-parcel disconnections and thermoception. Maximum statistic permutation (n = 10,000) was employed on permuted behavioural data and the original disconnection data to assess the distribution of maximum statistics under the null hypothesis. To adopt a more conservative approach, we applied a one-sided corrected threshold for statistical significance at p < 0.01 by identifying the 99th percentile of permutation-derived maximum statistics. Results are visualised with the BrainNet Viewer (http://www.nitrc.org/projects/bnv/). The image presents the disconnections significantly associated with reduced thermoception. Dots indicate regions at the endpoints of significant disconnections.