Abnormal Access of Axial Vibrotactile Input to Deafferented Somatosensory Cortex in Human Upper Limb Amputees

Abstract

We studied two human subjects with total deafferentation of one upper limb secondary to traumatic multiple cervical root avulsions. Both subjects developed a phantom limb and underwent elective amputation of the paralyzed, deafferentated limb. Psychophysical study revealed in each subject an area of skin in the pectoral region ipsilateral to the amputation where vibrotactile stimulation (VS) elicited referred sensations (RS) in the phantom limb. Positron emission tomography was then used to measure regional cerebral blood flow changes during VS of the pectoral region ipsilateral to the amputation with RS and during VS of a homologous part of the pectoral region adjacent to the intact arm without RS. A voxel-based correlation analysis was subsequently used to study functional connectivity. VS of the pectoral region adjacent to the intact arm was associated with activation of the dorsal part of the contralateral primary somatosensory cortex (S1) in a position consistent with the S1 trunk area. In contrast, VS of the pectoral region ipsilateral to the amputation with RS was associated with activation of the contralateral S1 that extended from the level of the trunk representation ventrally over distances of 20 and 12 mm, respectively, in the two subjects. The area of S1 activated during VS of the digits in a normal control subject was coextensive with the ventral S1 region abnormally activated during VS of the ectopic phantom representation in the two amputees, suggesting that the deafferented digit or hand/arm area had been activated by sensory input from the pectoral region. Correlation analysis showed an abnormal pattern of intrinsic connectivity within the deafferented S1 hand/arm area of both amputees. In one subject, the deafferented S1 was functionally connected with 3 times as many S1 voxels as the normally afferented S1. This abnormal functional connectivity extended in both the rostrocaudal and ventrodorsal dimensions. The results demonstrate that sensory input delivered to the axial body surface may gain access to the S1 hand/arm area in some humans who have suffered extensive deafferentation of this area. The findings are consistent with the hypothesis that deafferentation of an area of S1 may result in activation of previously dormant inputs from body surfaces represented in immediately adjacent parts of S1. The results also provide evidence that changes in functional connectivity between these adjacent areas of the cortex play a role in the somatotopic reorganization.

The Central Role of the Parietal Lobes in Consciousness

“…Recurrence from the peripheral site is thus not necessary to attain awareness of experience involved with the limb. This has been underlined by a PET study of two deafferented patients in comparison with a normal control subject (Kew et al, 1997); the patients both had regions on the body (in the chest area) whose stimulation could elicit experience in the hand region of the phantom limb. The regions observed to be activated in the brain of the patients during this experience included the relevant hand region of somatosensory cortex (together with superior parietal cortex, among others); this region was now being stimulated, it was suggested, by lateral cortico-cortical connections from the chest area in the somatosensory cortex.…”

Phantom limb pain in the human brain: Unraveling neural circuitries of phantom limb sensations using positron emission tomography

“…4 Extensive literature is available on the reorganization and electrophysiological correlates of phantom sensations, 5-10 and a few functional imaging studies exist on cortical reorganization in amputees. [11][12][13] Although the brain circuitries processing movement and pain in individuals with intact extremities are well described, 14,15 existent evidence for the generation and central nervous processing of the corresponding PL sensations of pain remain incomplete.…”

Why Brain Science is Essential to the Success of Hand Allotransplantation

“…These include an expanded representation of muscles of the residual limb [21,22], and in some cases a shift in the representation of muscles of the face into the former hand territory [23]. Likewise, the sensory representation of axial body surfaces [24] and/or the face [25][26][27] may intrude into the former S1 hand territory. Consistent with animal models [3], transcranial magnetic stimulation (TMS) studies suggest that reduced levels of intrahemispheric inhibition post-injury may play a key role in M1 reorganization [28,29].…”