Topographic Hierarchy

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A hallmark of somatosensory cortical plasticity is that topography dictates patterns of reorganization, with near neighbors in the sensory map prominently involved in the remodeling after peripheral deprivation. The most common type of reorganization is a reactivation of the region deprived of its dominant inputs by other intact inputs that are physically adjacent to the deprived representation. However, this is not, by any means, the rule. The source of the reactivating inputs can vary with different types of injury. Moreover, there appears to be a relatively rigid pecking order that governs which inputs are favored in the competition for the deprived space. The process by which inputs reactivate sensory representations after peripheral denervation is rather like the "if-then" clause used in computer programming. If any of the dominant inputs to a region are spared by the deafferentation procedure, they have preferential access to the deprived zone. If all dominant inputs are completely eliminated, then alternative inputs dominate the reactivation. Even among the alternatives, there seems to be a hierarchy so that some alternates are preferred over others. The evidence for such a pecking order is discussed below.

13.2.1 Dominant Inputs

For the most part, experimental protocols for sensory denervation completely eliminate the dominant inputs to a sensory representation. For example, nerve transection produces a robust and verifiable deprivation to a readily delineated region of the sensory epithelium, particularly in the core region of the deprived zone away from borders where the peripheral innervation from other sensory nerves may partially overlap the territory of the transected nerve.3 Amputation is an even better example of an easily demarcated sensory denervation.4 However, in other cases, it can be difficult to completely eliminate all sensory inputs to the targeted portion of the sensory map. This is particularly troublesome in studies that involve transection of the spinal tracts. The optimal strategy dictates that the spinal gray is left intact as much as possible, and thus sensory fibers that course near the gray matter often escape transection. However, these unwanted outcomes from studies of the effects of spinal cord injury have proven to be informative for questions regarding the hierarchy of deprivation-induced takeovers.

The data suggest compellingly that if even a few dominant sensory inputs are spared, their influence is amplified and the skin surface that they innervate takes over the full extent of the deprived territory. Jain et al.5 carefully documented cortical reactivation mediated by remaining inputs. In monkeys that had cervical dorsal column transection, tracers were injected into the skin near the peripheral nerve endings of forelimb sensory nerves to label the central sensory terminations. In normal monkeys, this technique yields patterns of labeling that reflect the precise topography of inputs from the skin of the forelimb.6-8 In monkeys with spinal cord transection, the tracer should be unable to cross the transection site in the dorsal column, and no terminal labeling should be apparent in the dorsal column nuclei, if the transection is complete. Another outcome would be expected if some of the sensory afferents that ascend in the dorsal columns are spared. Axons labeled by the subcutaneous injections would be observed crossing the lesion site in the dorsal spinal cord, and some labeling in the spared afferent terminals would be expected in the dorsal column nuclei. Both indices of spared sensory afferents were described by Jain et al.5 in monkeys that had incomplete dorsal column transection.

Using electrophysiological recording techniques, Jain and colleagues5 also mapped the region of primary somatosensory cortex (area 3b) affected by the dorsal column transection. The forelimb representation of primary somatosensory cortex of normal monkeys has been well characterized.9-11 As shown schematically in Figure 13.1, digit 1 is represented lateral-most and the other digits are represented

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