Morphological correlates of injury-induced reorganization in primate somatosensory cortex

Abstract

Background: Topographic reorganization of central maps following peripheral nerve injury has been well characterized. Despite extensive documentation of these physiological changes, the underlying anatomical correlates have yet to be fully explored. In this study, we used Golgi impregnation and light microscopy to assess dendritic morphology following denervation of the glabrous hand surface in adult primates.

Results: After survival durations that permit complete physiologically-defined reorganization, we find a systematic change in the dendritic arborization pattern of both layer II/III pyramidal and layer IV spiny stellate cells in the contralateral hand region of area 3b, compared to unaffected cortical areas. In general, our analyses indicate a progressive expansion of distal regions of the dendritic arbor with no appreciable changes proximally. This pattern of distal dendritic elaboration occurs for both basilar and apical dendrites.

Conclusions: These observations are consistent with the notion that latent inputs gain expression in reorganized cortex after nerve injury via their influence through contacts with more distally located termination sites.

Figure 1

Photomicrographs and reconstructions of Golgi-filled neurons. a: A typical layer II/III pyramidal cell used in the analysis of dendritic arborization. b: A typical layer IV spiny stellate cell. c,d: Reconstructions of a pyramidal and a stellate cell. Scale bar = 50 μm.

Figure 2

Dendritic arborization pattern in the distal sectors of layer II/III pyramidal cells. The figure depicts the extent of arborization as a function of distance from the cell body using a Sholl ring analysis. On average, basilar dendrites in deprived cortex are both more complex (increased number of intersections; Fig 2a) and longer (dendritic length; Fig 2b) than those from controls. Likewise, apical dendrites in deprived cortex are also more complex (intersections; Fig 2c) and longer (length; Fig 2d), compared to controls. All effects were statistically significant.

Figure 3

Dendritic arborization pattern in the distal sectors of layer II/III stellate cells. The figure depicts the extent of arborization as a function of distance from the cell body using a Sholl ring analysis. On average, basilar dendrites in deprived cortex are both more complex (increased number of intersections; Fig 3a) and longer (dendritic length; Fig 3b) than those from controls. Likewise, apical dendrites in deprived cortex are also more complex (intersections; Fig 3c) and longer (length; Fig 3d), compared to controls. All effects were statistically significant.

Figure 4

Comparison of basilar vs. apical effects for all cells analyzed. The figure illustrates that for both cell types (pyramidal and stellate) and metric of dendritic arborization (intersections and length), the magnitude of the effect was reliably larger for basilar dendrites than for apical dendrites.