Time-Dependent Changes in the Functional Organization of Somatosensory Cerebral Cortex following Digit Amputation in Adult Raccoons

Abstract

Surgical removal of the third forepaw digit in raccoons causes both long-term and short-term changes in functional organization within the digit 3 primary somatosensory (SmI) cortex. Previous studies have shown that 36-52 weeks following amputation in infant raccoons, neurons within the digit 3 cortical territory had become responsive to cutaneous stimulation of “new” forepaw regions adjoining the digit stump (Carson et al, 1981; Kelahan et al, 1980, 1981); the “novel” receptive fields (RFs) were often larger than normal and revealed no orderly somatotopic organization.

In the present study, the conical effects of digits a removal were examined in adult raccoons. Within 36 weeks after amputation, the digit 3 zone was also found to be reactivated by “novel” inputs from the forepaw, with no strictly topographic representation of the “new” skin fields. The basic features of cortical reactivation were very similar in animals amputated as adults and as infants, except (hat the former typically had larger neuronal RFs than the latter.

Short-term cortical changes were studied in adult raccoons within I day and between 1 and 4 weeks after amputation: Significant time-dependent differences were found in the reactivated digit 3 territory. Within 1 hr following amputation, some cells in the digit 3 zone began to respond to low-intensity cutaneous stimulation of “new” forepaw regions, limited almost exclusively to digits 2 and 4. Neuronal RFs tended to be larger than normal and showed no strictly topographic organization. One to 4 weeks following amputation, the condition of the digit 3 zone differed dramatically from that found immediately and long after amputation—the majority of responsive neurons could be excited only by high-intensity stimulation of small RFs on the digit 3 stump; relatively few cells were sensitive to low-intensity stimulation of adjacent, intact skin regions. Again, no true somatotopic organization was evident.

The combined results of these experiments indicate that within 36 weeks following removal of a digit in raccoons, the deprived Sml cortical sector undergoes a dynamic sequence of changes in functional organization: Neurons that are normally excited by stimulation of digit 3 first become responsive primarily to stimulation of digits 2 and 4 (within 1 day after amputation), then to the digit 3 stump (from at least 1-4 weeks after amputation), and finally again to digits 2 and 4 (within at least 36 weeks after amputation). Mechanisms are discussed that might be responsible for this time-dependent cortical plasticity, including the “unmasking” and strengthening of normally present, subthreshold afferent inputs, changes in the physiological properties of peripheral nerve fibers terminating in an amputation neuroma, and the growth of new central synaptic connections.