Neural correlates of evoked phantom limb sensations

Abstract

Previous work showed the existence of changes in the topographic organization within the somatosensory cortex (SI) in amputees with phantom limb pain, however, the link between nonpainful phantom sensations such as cramping or tingling or the percept of the limb and cortical changes is less clear. We used functional magnetic resonance imaging (fMRI) in a highly selective group of limb amputees who experienced inducible and reproducible nonpainful phantom sensations. A standardized procedure was used to locate body sites eliciting phantom sensations in each amputee. Selected body sites that could systematically evoke phantom sensations were stimulated using electrical pulses in order to induce phasic phantom sensations. Homologous body parts were also stimulated in a group of matched controls. Activations related to evoked phantom sensations were found bilaterally in SI and the intraparietal sulci (IPS), which significantly correlated with the intensity of evoked phantom sensations. In addition, we found differences in intra- and interhemispheric interaction between amputees and controls during evoked phantom sensations. We assume that phantom sensations might be associated with a functional decoupling between bilateral SI and IPS, possibly resulting from transcallosal reorganization mechanisms following amputation.

Keywords: Evoked phantom sensations; Functional magnetic resonance imaging; Functional reorganization; Unilateral limb amputees.

Fig. 1

Body templates of five limb amputees with phasic referred phantom sensations. Purple dots indicate the body sites that were electrically stimulated and green surfaces indicate areas in the missing limb in which amputees perceived phantom sensations. A1–A5: reference of amputee respective to data provided in Table 1. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

(A) Mean fMRI activation during electrical stimulation of ten body sites in the five amputees during inducing evoked phantom sensations. Functional activations can be seen bilaterally in the inferior parietal lobules (IPL), intraparietal sulci (IPS), inferior frontal cortices (BA44, BA45), premotor cortices, and in primary (SI) and secondary (SII) somatosensory cortices. (B) In the five yoked controls, mean fMRI activation during electrical stimulation of the same body sites as in (A). We found neural activity during electrical stimulation in the right inferior parietal lobule (IPL) and the right SII. Coordinates are displayed in the MNI 152 stereotaxic brain.

Fig. 3

(A) fMRI activation averaged over five amputees during electrical stimulation of ten body sites plotted on a 3D brain. The red lines delineate the postcentral sulcus. (B) Individual data points with, on the ordinate scale, the perceived intensity of evoked phantom sensations, and on the abscissa scale, the %BSC in left SI (top, left), right SI (top, right), left IPS (bottom, left) and right IPS (bottom right). Points with identical colors indicate the same participant. (B) Three-dimensional configuration of the modelled metric multidimensional scaling (MDS), showing distances matrices between variables related to phantom sensations shown in green (i.e. perceived intensity of evoked phantom sensations, unpleasantness of phantom sensations, MPI) and the %BSC in the four regions of interest depicted in (A), shown in blue. Superimposed on the MDS plots are the corresponding significant pairwise correlations using Spearman’s correlation coefficients rho (corrected for multiple testing using FDR). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Robust linear regressions between the %BSC in the right SI and the right IPS (A), between the %BSC in the right and left IPS (B) and between the right and left SI (C) in both amputees (grey) and controls (black).