A quantitative study of spinothalamic neurons in laminae I, III, and IV in lumbar and cervical segments of the rat spinal cord

Khulood M Al‐Khater,Andrew J Todd,Robert Kerr

doi:10.1002/cne.21811

Abstract

The major ascending outputs from superficial spinal dorsal horn consist of projection neurons in lamina I, together with neurons in laminae III–IV that express the neurokinin 1 receptor (NK1r) and have dendrites that enter the superficial laminae. Some neurons in each of these populations belong to the spinothalamic tract, which conveys nociceptive information via the thalamus to cortical areas involved in pain. A projection from the cervical superficial dorsal horn to the posterior triangular nucleus (PoT) has recently been identified. PoT is at the caudal end of the thalamus and was not included in injection sites in many previous retrograde tracing studies. We have injected various tracers (cholera toxin B subunit, Fluoro-Gold, and fluorescent latex microspheres) into the thalamus to estimate the number of spinothalamic neurons in each of these two populations, and to investigate their projection targets. Most lamina I and lamina III/IV NK1r-immunoreactive spinothalamic neurons in cervical and lumbar segments could be labeled from injections centered on PoT. Our results suggest that there are 90 lamina I spinothalamic neurons per side in C7 and 15 in L4 and that some of those in C7 only project to PoT. We found that 85% of the lamina III/IV NK1r-immunoreactive neurons in C6 and 17% of those in L5 belong to the spinothalamic tract, and these apparently project exclusively to the caudal thalamus, including PoT. Because PoT projects to second somatosensory and insular cortices, our results suggest that these are major targets for information conveyed by both these populations of spinothalamic neurons.

Highlights

The spinal dorsal horn receives a major input from primary afferent axons
The supraspinal projection targets of these two groups of cells have been studied most extensively in the rat and include the caudal ventrolateral medulla (CVLM), the lateral parabrachial area (LPb), the periaqueductal gray matter (PAG), and the thalamus (Menetrey et al, 1982, 1983; Cechetto et al, 1985; Hylden et al, 1989; Lima and Coimbra, 1988; 1989; Burstein et al, 1990; Lima et al, 1991; Ding et al, 1995; Todd et al, 2000; Spike et al, 2003; Gauriau and Bernard, 2004a). These projections are predominantly contralateral, a significant number of cells appear to project bilaterally (Spike et al, 2003). Both lamina I and lamina III–IV projection neurons that possess the neurokinin 1 receptor (NK1r) are densely innervated by substance P-containing primary afferent axons (Naim et al, 1997; Todd et al, 2002) and provide a route through which these afferents, which are known to be nociceptors (Lawson et al, 1997), can activate brain regions involved in pain mechanisms
There was no spread of tracer into the hypothalamus

Summary

Introduction

The spinal dorsal horn receives a major input from primary afferent axons. This input is organized according to modality, with nociceptive afferents terminating mainly in laminae I and II (Rexed, 1954; Todd and Koerber, 2005). The supraspinal projection targets of these two groups of cells have been studied most extensively in the rat and include the caudal ventrolateral medulla (CVLM), the lateral parabrachial area (LPb), the periaqueductal gray matter (PAG), and the thalamus (Menetrey et al, 1982, 1983; Cechetto et al, 1985; Hylden et al, 1989; Lima and Coimbra, 1988; 1989; Burstein et al, 1990; Lima et al, 1991; Ding et al, 1995; Todd et al, 2000; Spike et al, 2003; Gauriau and Bernard, 2004a) These projections are predominantly contralateral, a significant number of cells appear to project bilaterally (Spike et al, 2003). Both lamina I and lamina III–IV projection neurons that possess the NK1r are densely innervated by substance P-containing primary afferent axons (Naim et al, 1997; Todd et al, 2002) and provide a route through which these afferents, which are known to be nociceptors (Lawson et al, 1997), can activate brain regions involved in pain mechanisms

Methods

Results

Conclusion