Onset and development of intersegmental projections in the chick embryo spinal cord

Abstract

The ontogeny of intersegmental (propriospinal) projections was studied in the chick embryo spinal cord between embryonic day 2.5 and day 6. Our goals were 1) to determine the earliest projections of intersegmental interneurons between specific spinal regions and to establish the cell types involved; and 2) to follow the ontogeny of these projections during the early formative stages of spinal cord development. Studies were carried out in vitro by using an isolated spinal cord/brainstem preparation. Horseradish peroxidase injections were made either uni- or bilaterally at various levels of the spinal cord along the rostrocaudal axis of the embryo. HRP histochemistry was done on Vibratome sections with diaminobenzidine as the chromogen. Following unilateral injections at day 2.5, labelled commissural interneurons were found contralaterally and were confined to the injected segment. Subsequently, labelled cells were found progressively further away from the injected segment. By day 4.5 reciprocal projections extended between lumbar and brachial regions. Interneurons with intersegmental axonal projections were often undifferentiated, consisting of primitive unipolar or bipolar cells with little, if any, dendritic development. In some cases migrating interneurons could be retrogradely labelled from two or three segments away from the location of their translocating cell body. Anterograde Golgi-like labelling of early undifferentiated cells revealed growing axons, axonal terminals, and growth cones. Five or six reasonably distinct classes of intersegmental interneurons were identified based on their location, axonal projections, and morphology of dendritic arbors. These appeared to be segmentally and bilaterally arranged along the rostrocaudal axis of the spinal cord. The axons of some of these types of interneurons exhibited preferences in their longitudinal projections within the ventral and ventrolateral marginal zone at the very onset of pathway formation. From the present observations it can be concluded that intersegmental connectivity precedes the development of ascending and descending supraspinal, as well as primary afferent connections in the chick embryo spinal cord.

Somato-Dendritic Morphology Predicts Physiology for Neurons That Contribute to Several Kinds of Limb Movements

“…9). Morphological distinctions among spinal interneurons have often emphasized soma locations and axon projections and terminations (Bernhardt et al 1990;Hale et al 2001;Jankowska 1992;Li et al 2001;Nissen et al 2005;Oppenheim et al 1988;Roberts 2000;Yaginuma et al 1994); this seems appropriate given that axon terminations indicate probable synaptic targets. This approach to morphological categorization has also identified spinal neurons that have particular soma locations in early development (Bernhardt et al 1990;Hale et al 2001;Nissen et al 2005;Yaginuma et al 1994) and that play particular roles in axial movement control (Buchanan 2001;Grillner 2003;Higashijima et al 2004;Li et al 2001;Roberts 2000).…”

Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses

“…This finding is somewhat surprising, because studies of scratching have generally focused on ipsilateral neural circuitry. On the other hand, there are many propriospinal neurons with descending crossed axons in turtles (Kusuma and ten Donkelaar, 1980;Berkowitz and Stein, 1994a), as well as in lampreys (Buchanan, 1982;Ohta et al, 1991), embryonic tadpoles (see Roberts, 1989) embryonic newts (Harper and Roberts, 1993) goldfish (Fetcho, I99 1), lizards (ten Donkelaar and de Boer van Huizen, 1978;Kusuma and ten Donkelaar, 1980) chicks (Oppenheim et al, 1988) and mammals (Burton and Loewy, 1976;Molenaar, 1978;Molenaar and Kuypers, 1978;Matsushita et al, 1979;Menetrey et al, 1985;Hongo et al, 1989;Cassidy and Cabana, 1993). In addition, during turtle fictive scratching evoked by unilateral tactile stimulation, some hindlimb muscle nerves on the opposite side of the body are often activated with a clear rhythm ( Fig.…”

Expression patterns of engrailed‐like proteins in the chick embryo

“…These cells project axons from the ventrolatral wall of the hindbrain at stages 11-12, approximately 10 hr after AChE activity is observed in their cell bodies (Weikert et al, 1990). In the spinal cord the first axonal projections arise later, also from intersegmental neurons (for recent reports see Holley, 1982;Holley and Silver, 1987;Oppenheim et al, 1988;Schlosser and Tosney, 1988;Yagunima et al, 1990). In the spinal cord of zebrafish embryos En protein is expressed in interneurons (Hatta et al, 1991).…”