Growth of new brainstem connections in adult monkeys with massive sensory loss

Abstract

Somatotopic maps in the cortex and the thalamus of adult monkeys and humans reorganize in response to altered inputs. After loss of the sensory afferents from the forelimb in monkeys because of transection of the dorsal columns of the spinal cord, therapeutic amputation of an arm or transection of the dorsal roots of the peripheral nerves, the deprived portions of the hand and arm representations in primary somatosensory cortex (area 3b), become responsive to inputs from the face and any remaining afferents from the arm. Cortical and subcortical mechanisms that underlie this reorganization are uncertain and appear to be manifold. Here we show that the face afferents from the trigeminal nucleus of the brainstem sprout and grow into the cuneate nucleus in adult monkeys after lesions of the dorsal columns of the spinal cord or therapeutic amputation of an arm. This growth may underlie the large-scale expansion of the face representation into the hand region of somatosensory cortex that follows such deafferentations.primate ͉ somatosensory ͉ sprouting ͉ plasticity ͉ dorsal columns I n adult monkeys and other mammals, a loss of afferents from the skin is followed by reorganization of the somatosensory cortex so that lost inputs are replaced by intact inputs in the representation (1, 2). Massive losses of inputs lead to large-scale reorganizations such that the somatotopic boundaries in the cortex may shift by more than 10 mm (3, 4). Such reorganizations in sensory representations probably depend on multiple mechanisms, including the potentiation of remaining synapses, the unmasking of latent connections by disinhibition, and possibly the growth of axon arbors and dendrites (5-10). However, there is little direct evidence for the mechanisms that mediate largescale reorganizations. We presumed that neuronal growth may play an important role in reorganizations where response to the face inputs expands into the hand region of area 3b because the expansion of the receptive fields is beyond any known limits of normal spread of thalamocortical or corticocortical arbors (11)(12)(13)(14)(15). Moreover, our experiments showed that the emergence of responses to the stimulation of the chin in the deprived hand cortex takes 6-8 mo (3), a time compatible with the growth of new connections. Finally, at the lower brainstem levels, the chin representation in the trigeminal nucleus lies adjacent to the hand representation in the cuneate nucleus. A limited growth of horizontal connections is known to occur within deprived visual cortex of adult cats (10) and deprived somatosensory cortex of monkeys (9). In addition, in monkeys with arm amputations, there is evidence that afferents from the stump of the arm can grow a short distance from their normal terminations in the dorsal part of the cuneate nucleus of the brainstem to the nearby ventral part, where digit inputs normally terminate (16). The question that we address here is whether the growth of new connections in the brain is a critical component of the massive cortical reorganizat...

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