Morphological classes of spinothalamic lamina I neurons in the cat

Abstract

We examined the morphology and distribution of retrogradely labeled spinothalamic tract (STT) neurons in lamina I (the marginal zone) of the spinal dorsal horn after large injections of cholera toxin subunit B (CTb) or Fast Blue (FB) into the contralateral thalamus of cats. Based on the shape and orientation of the somata and proximal dendrites in horizontal sections, three distinct cell types were identified: (1) fusiform cells with small, spindle-shaped somata and bipolar, longitudinal dendritic arbors; (2) pyramidal cells with triangular somata and three main dendritic origins with primarily longitudinal arborizations; and (3) multipolar cells with larger, multiangular somata and four or more radiating dendritic arbors directed both longitudinally and mediolaterally. These three morphological types differed significantly in the number of primary dendrites and the size of the somata. Subclasses of multipolar cells were noted. Nearly all cells could be categorized into these three classes consistently in horizontal sections. A small number of cells with transitional shapes or with small, round somata were unclassified. The proportional distributions of these cell types were found to vary over the length of the spinal cord (from the third cervical through the coccygeal segments) in three cats. The overall proportions of cell types were 34% fusiform, 36% pyramidal, 25% multipolar, and 5% unclassified. The proportions of pyramidal and multipolar cells were strikingly higher within the C7-8 and L6-7 segments and lowest in the thoracic segments. In contrast, fusiform cells formed about 20% of the labeled lamina I STT population in the C7-8 and L6-7 segments but more than 60% in thoracic segments. Across all nine cats, the proportions were similar within the cervical (C5-8) and lumbosacral (L5-S1) enlargements, although considerable interanimal variability was noted. These distinct morphological types of lamina I STT cells with differential longitudinal distributions probably have different functional roles. They may correspond to the three main physiological classes of lamina I STT cells.

Nociceptive and thermoreceptive lamina I neurons are anatomically distinct

“…Even though there was variation in the fine details of the morphology of the neurons in this sample, which is similar to the variation observed in prior work [27][28][29][30] , overall there was an obvious correspondence between the functional category and the somatodendritic shape of these cells, which indicates that there are three major structural/functional types of lamina I neurons. Of the 18 NS cells identified, 12 were fusiform neurons, whereas 4 were multipolar and 2 were unclassified.…”

“…Abstr., 646.9, 1993), features indicating anatomical differences that could be reflected in the morphology of their cell bodies in lamina I. In horizontal sections, lamina I neurons in rat, cat and monkey can be anatomically categorized almost comprehensively into three basic, albeit variegated, cell types: fusiform, pyramidal, and multipolar [27][28][29][30] . The fusiform cells appear to have unmyelinated axons, whereas pyramidal and multipolar cells have myelinated axons; this matches the physiological difference in conduction velocities between NS cells and COLD or HPC cells.…”

“…We categorized the identified lamina I neurons anatomically as fusiform, pyramidal, multipolar and unclassified or transitional neurons, based on the morphological criteria of somatodendritic shape and orientation in horizontal sections (see below) that we have used in prior studies of retrogradely labeled lamina I spinothalamic cells in cat and monkey 29,30 . Even though there was variation in the fine details of the morphology of the neurons in this sample, which is similar to the variation observed in prior work [27][28][29][30] , overall there was an obvious correspondence between the functional category and the somatodendritic shape of these cells, which indicates that there are three major structural/functional types of lamina I neurons.…”

De novo expression of neurokinin‐1 receptors by spinoparabrachial lamina I pyramidal neurons following a peripheral nerve lesion

“…Lamina I neurons were originally classified into four types in the rat, independently of being projection or local circuit neurons Coimbra, 1983, 1986). Most recent studies focus on lamina I projection neurons, which have been classified into three populations, based on their morphological properties: fusiform, multipolar, and pyramidal (Yu et al, 1999(Yu et al, , 2005Zhang and Craig, 1997;Zhang et al, 1996). An intracellular physiological study allowed the correlation of morphological and physiological characteristics.…”

Substantia Gelatinosa of the Spinal Cord

“…More recent studies used a simplified classification of Lamina I neurons into three main types (fusiform, multipolar and pyramidal), based on the morphological properties of projection neurons in horizontal sections. This classification was originally established in the cat (Zhang et al, 1996) and primate (Zhang and Craig, 1997;Yu et al, 1999), but later adapted to the rat (Todd et al, 2002;Yu et al, 2005;Almarestani et al, 2007;Saeed and Ribeiro-da-Silva, 2013) (Fig. 3).…”