Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys

Abstract

Reorganization of somatosensory cortex after peripheral nerve damage typically has been attributed to cortical plasticity. Here we provide evidence that much of the large-scale cortical reorganization that occurs after a major loss of peripheral inputs reflects the sprouting or expansion of afferents from the remaining forelimb into deprived territories of the spinal cord and brainstem. We examined sensory afferent terminations in the spinal cord and brainstem, and determined the somatotopic organization of cortical area 3b in three adult monkeys with previous hand or forearm amputation, as veterinary treatment of forelimb injuries. In each monkey, the distribution of labeled sensory afferent terminations from the remaining parts of the fore-limb was much more extensive than the normal distribution of inputs from the forelimb, and extended into portions of the dorsal horn of the spinal cord and the cuneate nucleus of the brainstem related to the amputated hand. In the same animals, tactile stimulation of the forelimb activated much of the deprived hand representation in area 3b of cortex; the lateral portion of the deprived region in area 3B appeared to be reactivated by inputs from the face. These data provide important new evidence that one of the mechanisms subserving large scale reorganization in cortex is a relay of topographic changes that occur subcortically. Presumably, the expanded primary sensory inputs activate postsynaptic neurons that are normally driven by inputs from the hand so that the neurons now have receptive fields on the forearm. Since the topographic representation of the body is greatly magnified in the relay to cortex, the subcortical changes can result in dramatic cortical map changes.