The brain often reorganizes itself after damage to some of its sensory inputs, so that neurons that were responsive to the missing inputs come to respond to remaining inputs1. After the loss of somatosensory input from the hand, for example, the region of the somatosensory cortex on the opposite side of the brain that is normally responsive to touch on the hand becomes responsive, over months of recovery, to touch on the face or arm2,3,4,5,6.
When the brain reorganizes in this way, do the newly reactivated neurons signal that the sensations are coming from the location of the stimulated skin, or do they signal instead the location of their original but missing source of activation? This question has been tackled by Karen Davis and colleagues (page 385 of this issue7) by recording and stimulating brain responses with microelectrodes placed in the somatosensory thalamus of patients with missing limbs (Fig. 1, overleaf).
People with amputations often have the feeling that the missing limb is still present as a so-called phantom limb8. Furthermore, sensations on the missing limb can sometimes be evoked by touching ‘trigger zones’ on other parts of the body. For example, touching the face or remaining upper arm on the side of an arm amputee may produce sensations both of those body parts and of the missing hand9,10. A logical interpretation of these trigger zones is that touching the arm or the face activates neurons in the arm or the face territories in the brain, and the territories normally devoted to the hand.
According to this view, this type of brain reorganization is not beneficial, but instead contributes to the misperception that something is touching the phantom hand. Another possibility, however, is that the reactivated neurons devoted to a missing hand or foot become recalibrated by experience so that they come to signal stimuli on remaining body parts such as the hand or face. This, of course, would not explain trigger zones, but it would mean that the extensive brain reorganization that follows amputation is potentially useful.
People without amputations report appropriately localized sensations when sensory representations in the brain are stimulated electrically11. As part of a therapeutic procedure for amputees with pain, Davis and co-workers7 placed microelectrodes in normal parts of the somatosensory thalamus and in that part of the thalamus where neurons previously would have been activated by stimulating the missing limb. The investigators determined the regions of skin where light touch activated neurons recorded at various electrode locations, thereby defining the receptive fields of those neurons; and they electrically stimulated the same or nearby neurons to produce sensations, thus defining sensation fields.
In the normal, undeprived portions of the somatosensory thalamus, neurons had matching receptive fields and sensation fields. But in some amputees, those with notable phantom sensations, stimulating neurons with receptive fields on the stump of the missing limb produced sensations referred to the missing limb (Fig. 1). Thus, the brain had reorganized so that the territory of the missing limb in the thalamus had become responsive to the sensory inputs from the stump of the arm, whereas the activation of neurons in this territory continued to signal sensations on the missing limb.
This does not tell us how or where the sensations are generated, because the activated neurons in the thalamus in turn activate neurons elsewhere in the brain. But we now know that, for at least some people, deprived but reactivated neurons do not take on new and appropriate functions. Instead, these neurons continue to carry out their original roles. However, mismatched receptive and sensation fields were not found in all patients, suggesting that sometimes the reactivated neurons recalibrated to signal stump locations rather than locations on the missing limb.
The results of Davis and co-workers are consistent with limited observations of Woolsey et al.12 on the effects of stimulating somatosensory cortex in a patient with phantom leg pain. Electrical stimulation of the leg area of somatosensory cortex produced the sensations in the phantom leg. No studies were carried out on the possible reorganization of this cortex, but the observation that sensations were referred to the phantom leg indicates that that part of the cortex continued to signal the existence of the missing leg. We can conclude from these studies that neurons in the brain can retain their original functions long after they have had time to adopt new ones.
The thalamic stimulations and recordings in amputees provide support for another important conclusion. Most of the evidence for brain reorganization after injury or altered experience has come from studies of the more accessible sensory representations of the cortex on the surface of the brain. Information from receptors in the skin is relayed through sensory nerves to the lower brain stem, then to the thalamus, and next to the cortex. Depending on the circumstances of injury or experience, reorganizations of cortical maps could depend on modifications of neural circuitry that occur in the cortex, subcortical stations, or both. In monkeys with long-standing therapeutic forelimb amputation, the hand region of cortex is activated by intact inputs from the upper arm and face3. In these same monkeys, nerve fibres from the upper arm appear to have sprouted in the lower brain stem to innervate neurons normally contacted by nerve fibres from the missing hand.
From this it seems that the growth of new nerve terminals at the level of the first relay station activates the deprived brain-stem neurons, which project to and activate deprived neurons of the somatosensory thalamus, which in turn relay to the cortex. The extensive reactivation of deprived portions of the human thalamus demonstrates that there is a subcortical locus for much of the reorganization that follows limb amputation.
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