Damage to the right insula disrupts the perception of affective touch

  1. Louise P Kirsch  Is a corresponding author
  2. Sahba Besharati
  3. Christina Papadaki
  4. Laura Crucianelli
  5. Sara Bertagnoli
  6. Nick Ward
  7. Valentina Moro
  8. Paul M Jenkinson
  9. Aikaterini Fotopoulou
  1. Department of Clinical, Educational and Health Psychology, University College London, United Kingdom
  2. Institut des Systèmes Intelligents et de Robotique, Sorbonne Université, France
  3. Department of Psychology, University of the Witwatersrand, South Africa
  4. Department of Neuroscience, Karolinska Institutet, Sweden
  5. NPSY.Lab-VR, Department of Human Sciences, University of Verona, Italy
  6. Sobell Department of Motor Neuroscience and Movement Disorders, UCL Institute of Neurology, United Kingdom
  7. Department of Psychology, School of Life and Medical Sciences, University of Hertfordshire, United Kingdom
3 figures, 2 tables and 2 additional files

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 …

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 …

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 …

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 …

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 …

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 …

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 …

A. Lesions associated with decreased CT pleasantness sensitivity on the contralesional left forearm, in all patients (N = 35)
RegionNVoxelsXYZT-value
AALUnclassified104431192.88
Rolandic_Oper6348-9152.59
JHUUnclassified120431192.88
Superior_corona_radiata45248302.59
NatBrainLabUnclassified69431192.88
Arcuate_Anterior_Segment7248-9152.59
Corpus_Callosum11227282.56
Internal_Capsule15255272.56
B. Lesions associated with decreased CT pleasantness sensitivity on the contralesional left forearm, only in patients without sensory deficit (N = 25)
RegionNVoxelsXYZT-value
AALUnclassified4463316-43.08
Frontal_Inf_Oper849962.55
Frontal_Inf_Orb83525-82.77
Rolandic_Oper8837-4202.57
Insula59838−12123.06
Putamen11833-483.27
Heschl2444−1782.65
JHUUnclassified125433-483.27
Superior_corona_radiata8268242.57
External_capsule2233-573.06
Superior_longitudinal_fasciculus632-6242.57
NatBrainLabUnclassified127733-483.27
Arcuate_Anterior_Segment1137-5212.57
Inferior_Occipito_Frontal_Fasciculus1372-82.54
Internal_Capsule1268242.57
C. Lesions associated with decreased CT pleasantness sensitivity on the ipsilesional right forearm (N = 41)
RegionNVoxelsXYZT-value
AALFrontal_Inf_Oper5942992.76
Rolandic_Oper7945492.76
Insula3245382.70
JHUUnclassified17045492.76
NatBrainLabUnclassified17045492.76
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 …

Stroke Patients –RH (N = 59; 31 females)Healthy Controls - HC (N = 20, 11 females)Mann-Whitney TestNRH/NHC
MeanSDMeanSD
Age (years)65.8613.8763.0512.12U(78)=514.00, Z = -.857, p=0.391N = 59/20
Education (years)11.402.8714.752.82U(70)=211.50, Z = −3.906, p<0.001*N = 52/20
Days from onset16.9518.68--
Orientation2.800.41--
Nottingham on left arm (max 2)0.660.78--
Nottingham on right arm (max 2)20--
Proprioception (max 9)5.102.64--
MRC Left upper limb0.300.75--
Digit span forwards5.951.406.581.83U(66)=279.50, Z = 0.936, p=0.349N = 56/12
Digit span backwards3.501.554.751.28U(66)=177.00, Z = −2.621, p=0.009*N = 56/12
MOCA19.855.1828.191.92U(45)=5.50, Z = −4.271, p<0.001*N = 39/8
MOCA memory subscale2.921.784.001.60U(45)=95.00, Z = −1.769, p=0.077N = 39/8
Premorbid IQ-WTAR34.009.3549.111.69U(25)=3.00, Z = −4.037, p<0.001*N = 18/9
HADS depression5.753.493.132.19U(50)=150.00, Z = −2.593, p=0.010*N = 37/18
HADS anxiety8.024.336.063.01U(50)=208.00, Z = −1.409, p=0.159N = 37/18
FAB total score11.384.02--
Comb/razor test bias (%bias)−23.3727.06--
Bisiach one item test0.470.68--
Line crossing (max 36)22.5611.85--
Star cancelation (max 54)29.9318.23--
Copy0.871.20--
Representational drawing0.620.93--
Line bisection2.873.05--

Additional files

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.

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