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Obtaining and maintaining cortical hand representation as evidenced from acquired and congenital handlessness

  1. Daan B Wesselink
  2. Fiona MZ van den Heiligenberg
  3. Naveed Ejaz
  4. Harriet Dempsey-Jones
  5. Lucilla Cardinali
  6. Aurelie Tarall-Jozwiak
  7. Jörn Diedrichsen
  8. Tamar R Makin  Is a corresponding author
  1. University College London, United Kingdom
  2. University of Oxford, United Kingdom
  3. University of Western Ontario, Canada
  4. Istituto Italiano di Tecnologia, Italy
  5. Queen Mary’s Hospital, United Kingdom
Research Advance
Cite this article as: eLife 2019;8:e37227 doi: 10.7554/eLife.37227
3 figures, 1 table, 1 data set and 1 additional file

Figures

Figure 1 with 1 supplement
Similar representation in primary somatosensory cortex (SI) for amputees’ missing hand and controls’ nondominant hand, but not for congenital one-handers’ missing hand.

(A) Activity (averaged digit movement versus rest) in SI for amputees (n = 18), two-handed controls (n = 12), and congenital one-handers (n = 13). (B–C) Mean dissimilarity and typicality of the representational structure of contralateral SI activity for the three groups. (D) Representational dissimilarity matrices for the three groups. D1-D5 correspond to the five digits (thumb-little finger). (E) Two-dimensional projection of the representational structure (D) (using multi-dimensional scaling; note that this is included for visualisation purposes only and was not used for statistical analysis). Dissimilarity is reflected by distance in the two dimensions; individual digits are reflected by different colours (see colour key, bottom right); and ellipses reflect the between-subject standard error after Procrustes alignment. Please note the different scale for one-handers compared to amputees and controls. Abbreviations: a.u.: arbitrary unit; *: significant difference, after accounting for multiple comparisons.

https://doi.org/10.7554/eLife.37227.002
Figure 1—figure supplement 1
Similar representation in primary motor cortex (M1) for amputees’ missing hand and controls’ nondominant hand, but not for the congenital one-handers’ missing hand.

All annotations are detailed in main text Figure 1.

https://doi.org/10.7554/eLife.37227.003
Kinaesthetic sensations during individuated phantom hand movements in amputees correlate with typicality in the missing hand’s primary somatosensory cortex (SI).

Typicality is the correlation coefficient of the representational dissimilarity matrix (RDM) with an independent hand RDM in controls. Phantom kinaesthesia (A) shows the number of digits that produced a sensation of movement during volitional phantom digit movements, based on amputees’ self-reports. Grey and orange ranges show the mean and confidence intervals for typicality in one-handers and controls, respectively. The regression line is only presented for visualisation. Nonpainful phantom vividness (B) conveys the chronicity of the experience of the existence of a missing hand, where 0 indicates no sensations and 100 sensations identical to the intact hand.

https://doi.org/10.7554/eLife.37227.004
Similar ipsilateral hand representation in primary somatosensory cortex (SI) for amputees’ and controls’ intact hand.

(A–B) Mean dissimilarity and typicality of the representational structure of ipsilateral SI activity for the three groups. Both dissimilarity and typicality of ipsilateral hand representation indicate a difference between missing hand representation in congenital one-handers and amputees, independent of missing hand motor skill. The red error bars indicate the dissimilarity and typicality values (standard error of the mean) in a visual control area V5 for the same groups, designed to capture visuomotor representation that is not strictly somatosensory. While amputees and controls showed significantly greater digit representation in SI than V5 (both in terms of dissimilarity and typicality), congenital one-handers did not, further indicating reduced SI digit representation. Abbreviations: a.u.: arbitrary unit; *: significant difference; #: trending difference (.02 < p < 0.05).

https://doi.org/10.7554/eLife.37227.005

Tables

Table 1
Summary demographic details and phantom sensations.

Data is shown for amputees (AMP), controls (CTR) and congenital one-handers (1H). Congenital one-handers did not feel any phantom limb sensations. All controls have full kinaesthetic sensations. F: female, M: male. Side: side of missing hand; L: left, R: right. Amputation level: 1: shoulder, 2: above elbow; 3: at elbow; 4: below elbow; 5: at wrist. Kin: Phantom limb kinaesthesia (number of independent controllable parts of the hand), Viv: Chronic phantom limb vividness (0: no sensation, 100: intact hand’s vividness), Pain: Chronic phantom limb pain (0: no pain, 100: worst pain imaginable), AViv/APain: Acute Viv/Pain (on the scanning day), Std: standard deviation, ND: nondominant.

https://doi.org/10.7554/eLife.37227.006
AMPAge
(years)
SexAmputationPhantom sensations
SideYears sinceAge at
(years)
LevelKin
(0-5)
Viv
(0-100)
Pain
(0-100)
AViv
(0-100)
APain
(0-100)
Mean50.417.632.9358466521
St. dev.12.110.411.8238373023
A0144MR15292510010010050
A0253ML322125501006070
A0340ML1129241005010020
A0451ML32192510001000
A0527FR720425040600
A0671MR16552120856020
A0746MR18282370907050
A0856ML263045640100
A0964ML3133241004010010
A1058ML25623900800
A1128ML820544040200
A1257MR29282180908040
A1350FL149400000
A1452MR272525100808050
A1568MR264241160800
A1639FR9303435405030
A1758ML12464520650
A1846FL14324380305030
CTRAge
(years)
SexND hand1HAge
(years)
SexMissing hand
SideSideLevel
Mean45.3Mean45.7
St. dev.14.9St. dev.10.4
C0129MRH0141ML4
C0224FLH0237MR4
C0347FLH0331FL4
C0439MLH0460ML4
C0532MRH0539FL4
C0653FRH0654FL4
C0738FRH0734ML4
C0867MRH0863ML4
C0942MRH0944FR4
C1041MRH1055FL4
C1169MLH1146MR4
C1263FLH1237MR4
H1353FL4

Data availability

The data analysed in this study has been shared as a major dataset.

The following data sets were generated
  1. 1
    Open Science Framework
    1. B Wesselink Daan
    2. MZ van den Heiligenberg Fiona
    3. R Makin Tamar
    (2019)
    ID gmvua. Effects of arm amputation on motor control.

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