Segmental patterning of rat and chicken sympathetic preganglionic neurons: correlation between soma position and axon projection pathway

Abstract

The segmental organization of midthoracic rat and chicken sympathetic preganglionic neurons was examined by retrograde labeling in vivo and in vitro. The results demonstrate that individual sympathetic preganglionic neurons project only rostrally or caudally within the sympathetic chain, even though the spinal segment in which they reside provides innervation to both rostral and caudal ganglia. In addition, there is both a segmental and an intrasegmental pattern in the thoracic sympathetic column, in which the position of preganglionic neurons is related to the direction they project in the sympathetic chain. Thoracic sympathetic preganglionic neurons are organized into discrete segmental units, each of which exhibits an internal rostrocaudal polarity with respect to the direction of axon projection in the sympathetic chain. The rostrocaudal bias of this internal polarity is graded from segment to segment along the longitudinal axis. Since there is minimal overlap between thoracic segments, the transition from one segment to another entails a sharp change in the pathway choice of the preganglionic neurons. The organization of the preganglionic projections thus includes (1) segmental periodicity, (2) intrasegmental gradients of neuronal identity, and (3) an axial gradient of segment identity. The significance of these findings is twofold. First, they suggest a functional organization that may be related to the specificity of sympathetic reflex action. Second, they reveal a cellular organization that suggests an underlying segmental pattern in the developing spinal cord.

Segment-specific pattern of sympathetic preganglionic projections in the chicken embryo spinal cord is altered by retinoids

“…Here, the preganglionic sympathetic neurons exhibit segmental and intrasegmental patterns of differentiation with respect to their projection pathways in the sympathetic chain. In each segment, there is a segregation of the preganglionic neurons that project rostrally versus caudally in the chain, and the proportions and distributions of the two populations of neurons vary systematically from segment to segment (4). We now show that manipulation of retinoid signaling in the thoracic region alters selectively the number of rostrally projecting neurons, suggesting a mechanism by which retinoids can influence the segmentspecific pattern of sympathetic projections.…”

“…Normally, T2 is populated predominantly by rostrally projecting preganglionic neurons (Ͼ95%) whereas T6 contains only a minority of such neurons (Ͻ20%) (4). This difference reflects a progressive segmental shift in the proportion of rostrally and caudally projecting preganglionic neurons observed as one moves from rostral to caudal thoracic segments (4). Manipulations of retinoid signaling selectively altered the number of rostrally projecting preganglionic neurons compared with control (untreated or vehicle-treated).…”

“…1b). E10 embryos were killed, and the sympathetic preganglionic projections were labeled retrogradely in vitro with fluorescently tagged dextran amines as described (4). Because of occasional inaccuracy in somite counting in the older embryos, some of the caudally placed beads were found at T5 or T7, instead of T6.…”

Segmental Specificity of Chick Sympathetic Preganglionic Projections Is Influenced by Preganglionic Neurons from Neighboring Spinal Cord Segments

“…Projections of sympathetic preganglionic neurons in the sympathetic trunk of birds and mammals are segmentally specific (Langley 1892(Langley , 1904Lichtman et al, 1980;Rubin and Purves, 1980;Yip, 1990;Forehand et al, 1994;Yip et al, 1998). In the chick, for example, preganglionic neurons arising from the first thoracic spinal cord segment (T1) project predominantly in the rostral direction, whereas those arising from the last thoracic spinal cord segment (T7) project predominantly in the caudal direction.…”

“…Schwann cells, however, do not seem to be required for the formation of segmentally specific preganglionic projections because preganglionic projections are not affected by neural crest removal (Yip, 1987). Because each ganglion is innervated by preganglionic neurons arising from several spinal cord segments (Langley, 1904;Njå and Purves, 1977;Yip, 1986;Forehand, 1994), axons of preganglionic neurons from multiple spinal cord segments share the same pathway to arrive at their target ganglia. In the development of the nervous system it has been shown that axonal projections can be influenced by other axons.…”