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Ancestry of motor innervation to pectoral fin and forelimb.

Ma LH, Gilland E, Bass AH, Baker R - Nat Commun (2010)

Bottom Line: New and previous data for lobe-finned fish, a group that includes tetrapods, and more basal cartilaginous fish showed pectoral innervation that was consistent with a hindbrain-spinal origin of motoneurons.A phylogenetic analysis indicated that Hox gene modules were shared in fish and tetrapod pectoral systems.We propose that evolutionary shifts in Hox gene expression along the body axis provided a transcriptional mechanism allowing eventual decoupling of pectoral motoneurons from the hindbrain much like their target appendage gained independence from the head.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Neuroscience, NYU Langone Medical Center, New York, New York 10016, USA.

ABSTRACT
Motor innervation to the tetrapod forelimb and fish pectoral fin is assumed to share a conserved spinal cord origin, despite major structural and functional innovations of the appendage during the vertebrate water-to-land transition. In this paper, we present anatomical and embryological evidence showing that pectoral motoneurons also originate in the hindbrain among ray-finned fish. New and previous data for lobe-finned fish, a group that includes tetrapods, and more basal cartilaginous fish showed pectoral innervation that was consistent with a hindbrain-spinal origin of motoneurons. Together, these findings support a hindbrain-spinal phenotype as the ancestral vertebrate condition that originated as a postural adaptation for pectoral control of head orientation. A phylogenetic analysis indicated that Hox gene modules were shared in fish and tetrapod pectoral systems. We propose that evolutionary shifts in Hox gene expression along the body axis provided a transcriptional mechanism allowing eventual decoupling of pectoral motoneurons from the hindbrain much like their target appendage gained independence from the head.

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Embryonic alignment of pectoral and occipital motoneurons with nerves and myotomes in basal and derived actinopterygians.(a–d) Location of pectoral motoneurons and nerves in actinopterygians revealed by lipophilic dye labelling from fin buds. The pectoral motor column began at the level of myotomes (M) 2–3 in all species studied (vertical hatching marks hindbrain–spinal boundary; also see Figure 1b,e). (e–h) Double labelling with fluorescent dextrans from fin buds and M1–3 showed that the occipital motor column began one myotomal segment anterior to pectoral motoneurons. Horizontal hatching marks midline in f–h. (i) Alignment of myotomes, nerves and motoneurons (pectoral/red and occipital/grey) with phylogenetic relationships of actinopterygians studied here (right). Paddlefish innervation pattern was deduced from juvenile gross anatomy (Supplementary Fig. S1, S2) as individual roots were not clearly visualized using retrograde labelling. All images are dorsal views with anterior to the left. Scale bars are 50 μm. Specimen stages: a (10 days postfertilization (dpf)/~5.5 mm), b (2 dpf/~3 mm), c (100 dpf/~10 mm), d (9 dpf/~13 mm), e (18 dpf/~11 mm), f (4 dpf/~4 mm), g (115 dpf/~12 mm), h (11 dpf/~16 mm).
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f2: Embryonic alignment of pectoral and occipital motoneurons with nerves and myotomes in basal and derived actinopterygians.(a–d) Location of pectoral motoneurons and nerves in actinopterygians revealed by lipophilic dye labelling from fin buds. The pectoral motor column began at the level of myotomes (M) 2–3 in all species studied (vertical hatching marks hindbrain–spinal boundary; also see Figure 1b,e). (e–h) Double labelling with fluorescent dextrans from fin buds and M1–3 showed that the occipital motor column began one myotomal segment anterior to pectoral motoneurons. Horizontal hatching marks midline in f–h. (i) Alignment of myotomes, nerves and motoneurons (pectoral/red and occipital/grey) with phylogenetic relationships of actinopterygians studied here (right). Paddlefish innervation pattern was deduced from juvenile gross anatomy (Supplementary Fig. S1, S2) as individual roots were not clearly visualized using retrograde labelling. All images are dorsal views with anterior to the left. Scale bars are 50 μm. Specimen stages: a (10 days postfertilization (dpf)/~5.5 mm), b (2 dpf/~3 mm), c (100 dpf/~10 mm), d (9 dpf/~13 mm), e (18 dpf/~11 mm), f (4 dpf/~4 mm), g (115 dpf/~12 mm), h (11 dpf/~16 mm).

Mentions: Pectoral motoneurons were visualized by injecting a saturated solution of fluorescent lipophilic dye (DiD) into the fin bud that was incorporated into individual axons and diffused along the membrane to label the cell body. Subsequent confocal imaging revealed a consistent dual hindbrain–spinal origin of pectoral motoneurons in actinopterygians. Embryonic pectoral motor nuclei always extended as a column between myotomes (M) 2–3 and 5–6, with separate nerve roots projecting through each successive myotome, starting invariantly with M2 (Fig. 2a–d). Location of the embryonic cranio–vertebral17 and hindbrain–spinal16 junctions between M3 and 4 showed the pectoral column to be in both the caudal hindbrain and rostral spinal cord with the fin innervated by Oc and Sp nerves (Fig. 2a–d; Supplementary Movie 1). Taken together, our results indicate that basal and derived actinopterygians share a conserved blueprint, with a hindbrain–spinal pectoral motor nucleus innervating the fin via both Oc and Sp nerves.


Ancestry of motor innervation to pectoral fin and forelimb.

Ma LH, Gilland E, Bass AH, Baker R - Nat Commun (2010)

Embryonic alignment of pectoral and occipital motoneurons with nerves and myotomes in basal and derived actinopterygians.(a–d) Location of pectoral motoneurons and nerves in actinopterygians revealed by lipophilic dye labelling from fin buds. The pectoral motor column began at the level of myotomes (M) 2–3 in all species studied (vertical hatching marks hindbrain–spinal boundary; also see Figure 1b,e). (e–h) Double labelling with fluorescent dextrans from fin buds and M1–3 showed that the occipital motor column began one myotomal segment anterior to pectoral motoneurons. Horizontal hatching marks midline in f–h. (i) Alignment of myotomes, nerves and motoneurons (pectoral/red and occipital/grey) with phylogenetic relationships of actinopterygians studied here (right). Paddlefish innervation pattern was deduced from juvenile gross anatomy (Supplementary Fig. S1, S2) as individual roots were not clearly visualized using retrograde labelling. All images are dorsal views with anterior to the left. Scale bars are 50 μm. Specimen stages: a (10 days postfertilization (dpf)/~5.5 mm), b (2 dpf/~3 mm), c (100 dpf/~10 mm), d (9 dpf/~13 mm), e (18 dpf/~11 mm), f (4 dpf/~4 mm), g (115 dpf/~12 mm), h (11 dpf/~16 mm).
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f2: Embryonic alignment of pectoral and occipital motoneurons with nerves and myotomes in basal and derived actinopterygians.(a–d) Location of pectoral motoneurons and nerves in actinopterygians revealed by lipophilic dye labelling from fin buds. The pectoral motor column began at the level of myotomes (M) 2–3 in all species studied (vertical hatching marks hindbrain–spinal boundary; also see Figure 1b,e). (e–h) Double labelling with fluorescent dextrans from fin buds and M1–3 showed that the occipital motor column began one myotomal segment anterior to pectoral motoneurons. Horizontal hatching marks midline in f–h. (i) Alignment of myotomes, nerves and motoneurons (pectoral/red and occipital/grey) with phylogenetic relationships of actinopterygians studied here (right). Paddlefish innervation pattern was deduced from juvenile gross anatomy (Supplementary Fig. S1, S2) as individual roots were not clearly visualized using retrograde labelling. All images are dorsal views with anterior to the left. Scale bars are 50 μm. Specimen stages: a (10 days postfertilization (dpf)/~5.5 mm), b (2 dpf/~3 mm), c (100 dpf/~10 mm), d (9 dpf/~13 mm), e (18 dpf/~11 mm), f (4 dpf/~4 mm), g (115 dpf/~12 mm), h (11 dpf/~16 mm).
Mentions: Pectoral motoneurons were visualized by injecting a saturated solution of fluorescent lipophilic dye (DiD) into the fin bud that was incorporated into individual axons and diffused along the membrane to label the cell body. Subsequent confocal imaging revealed a consistent dual hindbrain–spinal origin of pectoral motoneurons in actinopterygians. Embryonic pectoral motor nuclei always extended as a column between myotomes (M) 2–3 and 5–6, with separate nerve roots projecting through each successive myotome, starting invariantly with M2 (Fig. 2a–d). Location of the embryonic cranio–vertebral17 and hindbrain–spinal16 junctions between M3 and 4 showed the pectoral column to be in both the caudal hindbrain and rostral spinal cord with the fin innervated by Oc and Sp nerves (Fig. 2a–d; Supplementary Movie 1). Taken together, our results indicate that basal and derived actinopterygians share a conserved blueprint, with a hindbrain–spinal pectoral motor nucleus innervating the fin via both Oc and Sp nerves.

Bottom Line: New and previous data for lobe-finned fish, a group that includes tetrapods, and more basal cartilaginous fish showed pectoral innervation that was consistent with a hindbrain-spinal origin of motoneurons.A phylogenetic analysis indicated that Hox gene modules were shared in fish and tetrapod pectoral systems.We propose that evolutionary shifts in Hox gene expression along the body axis provided a transcriptional mechanism allowing eventual decoupling of pectoral motoneurons from the hindbrain much like their target appendage gained independence from the head.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Neuroscience, NYU Langone Medical Center, New York, New York 10016, USA.

ABSTRACT
Motor innervation to the tetrapod forelimb and fish pectoral fin is assumed to share a conserved spinal cord origin, despite major structural and functional innovations of the appendage during the vertebrate water-to-land transition. In this paper, we present anatomical and embryological evidence showing that pectoral motoneurons also originate in the hindbrain among ray-finned fish. New and previous data for lobe-finned fish, a group that includes tetrapods, and more basal cartilaginous fish showed pectoral innervation that was consistent with a hindbrain-spinal origin of motoneurons. Together, these findings support a hindbrain-spinal phenotype as the ancestral vertebrate condition that originated as a postural adaptation for pectoral control of head orientation. A phylogenetic analysis indicated that Hox gene modules were shared in fish and tetrapod pectoral systems. We propose that evolutionary shifts in Hox gene expression along the body axis provided a transcriptional mechanism allowing eventual decoupling of pectoral motoneurons from the hindbrain much like their target appendage gained independence from the head.

Show MeSH