Developmental dynamics of functionally specific primary sensory afferent projections in the chicken embryo

Abstract

The central projections of specific subpopulations of lumbar primary afferents were selectively labeled with the lipophilic tracer DiI in fixed preparations of the chicken embryo. Muscle or cutaneous afferents were selectively labeled by applying DiI to identified peripheral nerves. Medial or lateral afferent populations were selectively labeled by partially lesioning the dorsal root. Muscle and cutaneous afferent populations each contribute to both the medial and the lateral afferent populations. Medial muscle afferents terminate in the intermediate zone and lateral motor column proximally, but only in the intermediate zone distally. Lateral muscle afferents terminate in a ventrolateral region of the dorsal horn both proximally and distally. Medial cutaneous afferents terminate predominantly in lamina III, but a few terminate in the medial region of the intermediate zone. Lateral cutaneous afferents terminate in lamina II and in a ventrolateral region of the dorsal horn. On the basis of the principle termination patterns, specific termination fields were defined and related to the classical cytoarchitectonics of the spinal gray matter. Differential retrograde tracing from the spinal cord with fluorescent dextran-amines demonstrated that the medial afferents originate from the earlier-generated ventrolateral population of large sensory cell bodies, while the lateral afferents originate from the later-generated dorsomedial population of small sensory cell bodies. The medial afferents establish their central projections earlier than the lateral afferents, but for each subpopulation the initial pattern of termination prefigures the mature pattern, throughout the segmental range of the collaterals. Birthdating with 3H-thymidine showed that potential target neurons in the different terminal fields within the dorsal horn are born at different times. In particular, interneurons in lamina II are born after those in lamina III, paralleling the early and late termination of cutaneous afferents in these laminae. Our observations support the notion that primary afferents recognize specific cues in the spinal cord, but also implicate the relative timing of afferent and target differentiation as an important determinant of primary afferent termination patterns.

Development of vestibular afferent projections into the hindbrain and their central targets

“…Such a scheme of distribution is similar to dorsal root ganglion neurons whose different subpopulations, conveying different sensory information, are overlapping at the level of the ganglion [65]. However, these neurons sort out very sharply into modality-specific laminar projections into the spinal cord such as the Lissauer's tract and dorsal columns [27].…”

The SynCAM synaptic cell adhesion molecules are involved in sensory axon pathfinding by regulating axon-axon contacts

“…At HH30 and HH34, SynCAMs were expressed in a subtype-specific manner in DRG neurons. In chicken, like in human, subpopulations of sensory neurons are segregated to different positions in the DRG (Eide and Glover, 1997). SynCAM1 mRNA (Fig.…”

“…7D). Nociceptive collaterals, which normally extend from the lateral dorsal funiculus into laminae I and II of the dorsal horn (Eide and Glover, 1997;Perrin et al, 2001), were found to overshoot their target and project to lamina III, or even to cross the midline (Fig. 7E-G).…”

“…At HH30 and HH34, SynCAM1 (J) and SynCAM2 (K) expression was restricted to the dorsomedial and the ventrolateral region of the DRG, respectively. In chick, unlike in rodents, where neurons are arranged randomly, subpopulations of sensory neurons are segregated to different domains of the DRG (Eide and Glover, 1997). Insets depict staining for TrkA (J) and TrkC (K).…”

Axonal projections of mechanoreceptive dorsal root ganglion neurons depend on Ret

“…Proprioceptive afferents pass through the medial part of the dorsal horn without branching and reach the ventral spinal cord, where they finally synapse to motoneurons (Caspary and Anderson, 2003). Whereas the axon terminals of nociceptive neurons are strictly confined to the dorsal horn and do not enter the ventral spinal cord, proprioceptive central afferents do not branch in the dorsal horn and are able to invade the ventral spinal cord (Eide and Glover, 1997). Thus, it has been suggested that repulsive and attractive cues residing in the dorsal horn and/or the ventral spinal cord guide each afferent to the proper region (Perrin et al, 2001;Sharma and Frank, 1998).…”