The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord

Abstract

Transganglionic transport of wheatgerm agglutinin conjugated horse-radish peroxidase (WGA-HRP) was used to reveal the central distribution of terminals of primary afferent fibers from peripheral nerves innervating the hind leg of the rat. In separate experiments the sizes and locations of cutaneous peripheral receptive fields were determined by electrophysiological recording techniques for each of the nerves that had been labeled with WGA-HRP. By using digital image analysis, the sizes and positions of the peripheral receptive fields were correlated with the areas of superficial dorsal horn occupied by terminals of primary afferents from each of these receptive fields. Data were obtained from the posterior cutaneous nerve of the thigh, lateral sural, sural, saphenous, superficial peroneal, and tibial nerves. The subdivisions of the sciatic nerve, the sural, lateral sural, superficial peroneal, and tibial nerves each projected to a separate and distinct region of the superficial dorsal horn and collectively formed a "U"-shaped zone of terminal labeling extending from lumbar spinal segments L2 to the caudal portions of L5. The gap in the "U" extended from L2 to the L3-4 boundary and was occupied by terminals from the saphenous nerve. Collectively, all primary afferents supplying the hindlimb occupied the medial 3/4 of the superficial dorsal horn with terminals from the tibial nerve lying most medially and occupying the largest of all the terminal fields. Afferents from the superficial peroneal lay in a zone between the medially situated tibial zone and the more laterally placed sural zone. Afferents from the posterior cutaneous nerve were located most caudally and laterally. Terminal fields from the posterior cutaneous and saphenous nerves differed from the others in having split representations caused presumably by their proximity to the mid-axial line of the limb. Comparisons between the peripheral and the central representations of each nerve revealed that 1 mm2 of surface area of the superficial dorsal horn serves approximately 600-900 mm2 of hairy skin and roughly 300 mm2 of glabrous skin. The vast majority of terminal labeling observed in the dorsal horn was found in the marginal layer and substantia gelatinosa, suggesting that small diameter afferents have an orderly somatotopic arrangement in which each portion of the skin surface is innervated by afferent fibers that terminate in preferred localities within the dorsal horn.

Induction of Fos protein expression in spinal cord neurons of tumour-bearing rats

“…Most labelled neurons evoked by the tumour graft were detected ipsilaterally at the L3-L5 levels, consistent with the somatotopic organization of the primary afferent fibres that innervate the grafted hind limb (Molander et al, 1984;Swett and Woolf, 1985). Because spinal Fos expression reflects neuronal activity (Hunt et al, 1987;Morgan et al, 1987), the present observations demonstrate the existence of a primary afferent transmission from the peripheral tumour and/or the adjacent tissues to the spinal cord.…”

Distinct Populations of Spinal Cord Lamina II Interneurons Expressing G-Protein-Gated Potassium Channels

“…Substance P labeling has been found to be intense in lamina IIo, suggesting that peptidergic PAFs make considerable synaptic input to this sublamina (Doly et al, 2004). In addition, some studies have shown that lamina IIi is prominently labeled by isolectin-B4 (IB4), an ␣-D-galactose-binding lectin from Griffonia (Bandeiraea) simplicifolia that preferentially labels nonpeptidergic fine-caliber PAFs (Swett and Woolf, 1985;Silverman and Kruger, 1988a,b;Molliver et al, 1997;Bennett et al, 1998). Other groups, however, have shown termination of IB4-reactive fibers in both laminas IIo and IIi (Wang et al, 1994), whereas a relatively recent transganglionic labeling study demonstrated prominent labeling of mouse lamina IIo with IB4 (Woodbury et al, 2000).…”

Stereological and somatotopic analysis of the spinal microglial response to peripheral nerve injury

“…However, there is a small but distinct spread of microglia into the intact sural territory of the dorsal horn in L4/5 which can be clearly seen in the lower panel where the CTB and IB4 labelling (left) have been separated from the microglial labeling (right). However, the characteristic 'saphenous notch' (the gap in CTB labelling in L3 in both naïve and SNI where the adjacent saphenous nerve central terminals project) (Swett and Woolf, 1985) is also present in the microglial labeling in the SNI example. Therefore, there is a spread of microglial activity outside the injured central terminal fields following SNI, but it is restricted to the central terminals of the intact branch of the sciatic nerve.…”

“…The central projections of peripheral sensory nerves to lamina II of the dorsal horn are somatotopically arranged (Swett and Woolf, 1985;Molander and Grant, 1986;Woolf and Fitzgerald, 1986;Shortland et al, 1989) (Fig. 5).…”