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.

Cortical reorganization and phantom phenomena in congenital and traumatic upper-extremity amputees

“…In addition, the clinical samples used in previous research might be very different from our self-selected amputee sample. Our data indicate that the loss of input from a limb in the pre-or early postnatal stage does not lead to significant reorganizational changes in SI (as one might deduce from animal studies; see Merzenich et al 1984;Pons et al 1991;Florence and Kaas 1995)]. …”

“…Although we have thus far addressed only the functional reorganization in SI after amputation, it is quite possible that the original locus of these alterations is not in somatosensory cortex but is rather at the level of the spinal cord or the thalamus (Howe 1983;Florence and Kaas 1995;Jain et al 1997). Furthermore, the role of interhemispheric transfer requires investigation.…”

Bilateral behavioral and regional cerebral blood flow changes during painful peripheral mononeuropathy in the rat

“…Previous experiments in animals have shown that reorganization can occur at the cortical level following peripheral injury (Pons et al, 1988(Pons et al, ,1991Guilbaud et al, 1991Guilbaud et al, ,1992Recanzone et al, 1992;Mao et al, 1993;Florence and Kaas, 1995;Chen et al, 1998). Guilbaud et al (1991) described abnormal spontaneous 'paroxysmal' discharges in S1 neurons that occurred without stimulation and which lasted up to 5 minutes in CCI animals.…”

Somatosensory cortical plasticity: recruiting silenced barrels by active whiskers

“…Cortical plasticity has also been reported in humans with referred phantom sensations after spinal cord injury (Mackert et al, 2003;Moore et al, 2000). While some of these effects may be attributed to changes in subcortical somatosensory pathways and reflection of these changes in the somatosensory cortex (Florence and Kaas, 1995;Kaas, 2002;Wall et al, 2002), several lines of evidence indicate that alterations in intracortical pathways play a major role in functional plasticity. Interestingly, different forms of cortical plasticity are manifested during early stages of cortical development and throughout maturity.…”