Damage to the right insula disrupts the perception of affective touch
- Department of Clinical, Educational and Health Psychology, University College London, United Kingdom
- Institut des Systèmes Intelligents et de Robotique, Sorbonne Université, France
- Department of Psychology, University of the Witwatersrand, South Africa
- Department of Neuroscience, Karolinska Institutet, Sweden
- NPSY.Lab-VR, Department of Human Sciences, University of Verona, Italy
- Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, United Kingdom
- Department of Psychology, School of Life and Medical Sciences, University of Hertfordshire, United Kingdom
Figures
Figure 1 with 2 supplements
Behavioural Results.
(A) Average intensity ratings on the contralesional left forearm (NRH = 39, NHC = 20), (B) Average intensity ratings on the ipsilesional right forearm (NRH = 20, NHC = 20), (C) Average pleasantness ratings on the contralesional left forearm (NRH = 35, NHC = 20), (D) Average pleasantness ratings on the ipsilesional right forearm (NRH = 41, NHC = 20), for CT-optimal and CT suboptimal touch. Stroke patients (RH) are depicted in dark gray, Healthy controls (HC) in light gray. Error bars represent the standard error of the mean. *depicts significant comparison, p<0.05.
Figure 1—figure supplement 1
Average pleasantness ratings on the contralesional left forearm for patients with intact tactile perception in dark gray (NRH = 25).
Results for healthy controls are the same as presented in Figure 1. C, in light gray (NHC = 20). Error bars represent the standard error of the mean. Average pleasantness ratings on the contralesional left forearm for patients with intact tactile perception in dark gray (NRH = 25). Results for healthy controls are the same as presented in Figure 1. C, in light gray (NHC = 20). Error bars represent the standard error of the mean.
Figure 1—figure supplement 2
Average pleasantness ratings for imaginary touch.
Patients rated how pleasant it would be to be touched by a typically pleasant material (i.e. velvet) and a typically unpleasant fabric (i.e. sandpaper). Error bars represent the standard error of the mean.
Figure 2 with 1 supplement
Lesions associated with decreased CT pleasantness sensitivity.
(A) Lesions associated with decreased CT pleasantness sensitivity on the contralesional left forearm, in all patients (N = 35). (B) Lesions associated with decreased CT pleasantness sensitivity on the contralesional left forearm, only in patients without sensory deficit on the left (N = 25). (C) Lesions associated with decreased CT pleasantness sensitivity on the ipsilesional right forearm (N = 41). The numbers above the brain slices indicate the corresponding MNI axial coordinates. L = Left; R = Right; The second row represents heat maps of the voxels with power enough to detect significant results, at α = 0.01, FDR-corrected. Different colors represent the area under the ROC curve (AUROC) scores, ranging from 0.2 to 0.6.
Figure 2—figure supplement 1
Lesions Overlaps.
(A) Lesions overlap map for patients with negative CT pleasantness sensitivity on the left contralesional forearm, among all patients (N = 10). Out of the 10 patients that showed a negative CT pleasantness sensitivity on the contralesional forearm (among all patients, N = 35), 8 of them had a lesion to the rolandic operculum cluster (X = 48, Y=-9, Z = 15); and for the two remaining patients, one had a more focal deep lesions (amygdala, putamen, thalamus), that could still be on the posterior insula track; and the other had an insula lesion but more frontal. (B) Lesions overlap map for patients with negative CT pleasantness sensitivity on the left contralesional forearm, only in patients without sensory deficit (N = 6). When taking into account only patients without sensory deficit, out of the six patients that showed a negative CT pleasantness sensitivity on the contralesional forearm (among patients without sensory deficit, N = 25), five had a lesion to the posterior insula cluster (X = 38, Y=-12, Z = 12), and the other had a more focal deep lesion (amygdala, putamen, thalamus) (C) Lesions overlap map for patients with negative CT pleasantness sensitivity on the right ipsilesional forearm (N = 18). Out of the 18 patients with a negative CT pleasantness sensitivity on the ipsilesional forearm, 15 had a lesion of the anterior insula cluster (X = 45, Y = 3, Z = 8); and the three remaining had a lesion to the insula, but not on that specific cluster. An overlay heat map of participants’ lesions was calculated from all lesions and superimposed on the chi2bet template brain using MRICron (Rorden et al., 2007).
Figure 3
Experimental design and timeline.
1. Participants were first asked to answer two hypothetical questions about imagined touch: ‘How pleasant would it be to be touched by velvet on your skin’ (typically pleasant) and ‘How pleasant would it be to be touched by sandpaper on your skin?’ (typically unpleasant). Participants were asked to answer using the vertical 0 to 10 pleasantness scale. 2. Participants were then asked to put on a blindfold at the onset of each trial before the experimenter delivered the touch on the left or right forearm at CT-optimal (CT touch) or CT-suboptimal velocities (nonCT touch; pseudorandomized), each touch lasted for 3 s and was repeated twice with a one second break in between. After each touch, blindfold was removed so participants could rate the touch on two scales: Intensity = How well they felt the touch; and Pleasantness = How pleasant was the touch, each on a vertical scale ranging from 0, not at all, to 10, extremely. After ratings were recorded, the participant was asked to put the blindfold back before starting the next trial.
Tables
Table 1
Number of significant voxels (from the atlas of gray matter – AAL – and white matter – JHU – and NatBrainLab’s atlas) resulting from the VLSM analyses.
A. with the CT pleasantness sensitivity scores for the contralesional left forearm as predictor, in all patients (N = 35); B. with the CT pleasantness sensitivity scores for the contralesional left forearm as predictor, only in patients without sensory deficit, N = 25; C. with the CT pleasantness sensitivity scores for the ipsilesional right forearm as predictor (N = 41).
| A. Lesions associated with decreased CT pleasantness sensitivity on the contralesional left forearm, in all patients (N = 35) | ||||||
|---|---|---|---|---|---|---|
| Region | NVoxels | X | Y | Z | T-value | |
| AAL | Unclassified | 104 | 43 | 1 | 19 | 2.88 |
| Rolandic_Oper | 63 | 48 | -9 | 15 | 2.59 | |
| JHU | Unclassified | 120 | 43 | 1 | 19 | 2.88 |
| Superior_corona_radiata | 45 | 24 | 8 | 30 | 2.59 | |
| NatBrainLab | Unclassified | 69 | 43 | 1 | 19 | 2.88 |
| Arcuate_Anterior_Segment | 72 | 48 | -9 | 15 | 2.59 | |
| Corpus_Callosum | 11 | 22 | 7 | 28 | 2.56 | |
| Internal_Capsule | 15 | 25 | 5 | 27 | 2.56 | |
| B. Lesions associated with decreased CT pleasantness sensitivity on the contralesional left forearm, only in patients without sensory deficit (N = 25) | ||||||
| Region | NVoxels | X | Y | Z | T-value | |
| AAL | Unclassified | 446 | 33 | 16 | -4 | 3.08 |
| Frontal_Inf_Oper | 8 | 49 | 9 | 6 | 2.55 | |
| Frontal_Inf_Orb | 8 | 35 | 25 | -8 | 2.77 | |
| Rolandic_Oper | 88 | 37 | -4 | 20 | 2.57 | |
| Insula | 598 | 38 | −12 | 12 | 3.06 | |
| Putamen | 118 | 33 | -4 | 8 | 3.27 | |
| Heschl | 24 | 44 | −17 | 8 | 2.65 | |
| JHU | Unclassified | 1254 | 33 | -4 | 8 | 3.27 |
| Superior_corona_radiata | 8 | 26 | 8 | 24 | 2.57 | |
| External_capsule | 22 | 33 | -5 | 7 | 3.06 | |
| Superior_longitudinal_fasciculus | 6 | 32 | -6 | 24 | 2.57 | |
| NatBrainLab | Unclassified | 1277 | 33 | -4 | 8 | 3.27 |
| Arcuate_Anterior_Segment | 11 | 37 | -5 | 21 | 2.57 | |
| Inferior_Occipito_Frontal_Fasciculus | 1 | 37 | 2 | -8 | 2.54 | |
| Internal_Capsule | 1 | 26 | 8 | 24 | 2.57 | |
| C. Lesions associated with decreased CT pleasantness sensitivity on the ipsilesional right forearm (N = 41) | ||||||
| Region | NVoxels | X | Y | Z | T-value | |
| AAL | Frontal_Inf_Oper | 59 | 42 | 9 | 9 | 2.76 |
| Rolandic_Oper | 79 | 45 | 4 | 9 | 2.76 | |
| Insula | 32 | 45 | 3 | 8 | 2.70 | |
| JHU | Unclassified | 170 | 45 | 4 | 9 | 2.76 |
| NatBrainLab | Unclassified | 170 | 45 | 4 | 9 | 2.76 |
Table 2
Summary of demographics and neuropsychological data.
Description: Nottingham = Light Touch subscale of the Revised Nottingham Sensory Assessment (rNSA; Lincoln et al., 1998; score overall for each arm with 0: no sensation; 1: slightly impaired; 2: no deficit); MRC = Medical Research Council scale (Saunders, 1986); MOCA = The Montreal Cognitive Assessment (Nasreddine et al., 2005); FAB = Frontal Assessment Battery (Dubois et al., 2000); Premorbid IQ-WTAR = Wechsler Test of Adult Reading (Wechsler, 2001); HADS = Hospital Anxiety and Depression scale (Zigmond and Snaith, 1983); Comb/razor test = tests of personal neglect (McIntosh et al., 2000); Bisiach one item test = test of personal neglect; line crossing, star cancellation, copy and representational drawing = conventional sub-tests of Behavioural Inattention Test (Wilson et al., 1987). Dashed line indicates not applicable. Due to several clinical constraints (e.g. fatigue, acceptance and time constraints), we have a number of missing data on these tests. Specific numbers are indicated in the right column. NRH = number of right hemisphere stroke patients having fully completed the corresponding test. NHC = number of healthy controls having fully completed the corresponding test. * Significant difference between groups, p<0.05.
| Stroke Patients –RH (N = 59; 31 females) | Healthy Controls - HC (N = 20, 11 females) | Mann-Whitney Test | NRH/NHC | |||
|---|---|---|---|---|---|---|
| Mean | SD | Mean | SD | |||
| Age (years) | 65.86 | 13.87 | 63.05 | 12.12 | U(78)=514.00, Z = -.857, p=0.391 | N = 59/20 |
| Education (years) | 11.40 | 2.87 | 14.75 | 2.82 | U(70)=211.50, Z = −3.906, p<0.001* | N = 52/20 |
| Days from onset | 16.95 | 18.68 | - | - | ||
| Orientation | 2.80 | 0.41 | - | - | ||
| Nottingham on left arm (max 2) | 0.66 | 0.78 | - | - | ||
| Nottingham on right arm (max 2) | 2 | 0 | - | - | ||
| Proprioception (max 9) | 5.10 | 2.64 | - | - | ||
| MRC Left upper limb | 0.30 | 0.75 | - | - | ||
| Digit span forwards | 5.95 | 1.40 | 6.58 | 1.83 | U(66)=279.50, Z = 0.936, p=0.349 | N = 56/12 |
| Digit span backwards | 3.50 | 1.55 | 4.75 | 1.28 | U(66)=177.00, Z = −2.621, p=0.009* | N = 56/12 |
| MOCA | 19.85 | 5.18 | 28.19 | 1.92 | U(45)=5.50, Z = −4.271, p<0.001* | N = 39/8 |
| MOCA memory subscale | 2.92 | 1.78 | 4.00 | 1.60 | U(45)=95.00, Z = −1.769, p=0.077 | N = 39/8 |
| Premorbid IQ-WTAR | 34.00 | 9.35 | 49.11 | 1.69 | U(25)=3.00, Z = −4.037, p<0.001* | N = 18/9 |
| HADS depression | 5.75 | 3.49 | 3.13 | 2.19 | U(50)=150.00, Z = −2.593, p=0.010* | N = 37/18 |
| HADS anxiety | 8.02 | 4.33 | 6.06 | 3.01 | U(50)=208.00, Z = −1.409, p=0.159 | N = 37/18 |
| FAB total score | 11.38 | 4.02 | - | - | ||
| Comb/razor test bias (%bias) | −23.37 | 27.06 | - | - | ||
| Bisiach one item test | 0.47 | 0.68 | - | - | ||
| Line crossing (max 36) | 22.56 | 11.85 | - | - | ||
| Star cancelation (max 54) | 29.93 | 18.23 | - | - | ||
| Copy | 0.87 | 1.20 | - | - | ||
| Representational drawing | 0.62 | 0.93 | - | - | ||
| Line bisection | 2.87 | 3.05 | - | - | ||
Additional files
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Supplementary file 1
Number of significant voxels (from the atlas of gray matter – AAL – and white matter – JHU – and NatBrainLab’s atlas) resulting from the VLSM analysis with the general pleasantness sensitivity scores (velvet-sandpaper average pleasantness ratings), N = 36.
As control for a general pleasantness deficit, patients rated how pleasant it would be to be touched by a typically pleasant material (i.e. velvet, Mpleasantness rating = 6.91, SD = 1.88) and a typically unpleasant fabric (i.e. sandpaper, Mpleasantness rating = 0.33, SD = 0.93). Similarly, as for CT pleasantness sensitivity, top-down tactile pleasantness sensitivity was computed as the difference between pleasant (velvet) and unpleasant pleasantness ratings (sandpaper), for each patient. We considered the same patients as for the CT pleasantness sensitivity VLSM analysis (N = 36 as we had missing data for 5 of them) and ran a VLSM analysis with this top-down tactile pleasantness sensitivity.
- https://cdn.elifesciences.org/articles/47895/elife-47895-supp1-v2.docx
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Damage to the right insula disrupts the perception of affective touch
eLife 9:e47895.
https://doi.org/10.7554/eLife.47895
