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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 precerebellar, pectoral and other hindbrain neurons in transgenic zebrafish.(a) Rhombomere (r) 7–8 YFP expression in hoxb4a enhancer trap line. (b) Reticular (labelled from the spinal cord; red) and YFP (green) neurons showed hindbrain–spinal cord boundary between myotomes (M) 3–4. (c) Half of the pectoral column (labelled from fin bud; red) was within the hindbrain. (d) Occipital motor column (labelled from M1–3/occipital) extended to mid r8, one segment rostral to pectoral motoneurons. (e–g) Dorsal composites (e) and selected confocal planes (f, g) of pectoral (labelled from fin buds; red), inferior olive (IO) and Area II (AII) (labelled from the cerebellum; magenta) neurons in islet-GFP background (green), showing the relative position of pectoral motoneurons with major neuronal subgroups. GFP in this line is expressed in all hindbrain motoneurons, except abducens and pectoral. (h) Vagal (X) and more ventral occipital (Oc) motor columns that extended from spinal cord into the hindbrain (also see f, g). (i) Alignment of pectoral motoneurons (Pec) with other neuronal and anatomical landmarks. Pectoral motoneurons in zebrafish were located across the hindbrain–spinal cord boundary at the level of M3–5 (see Figure 2). Hindbrain motoneurons are located immediately caudal to the inferior olive, below the vagal nucleus (X) and hindbrain commissure (HB com). They are part of the occipital motor column (Oc Mns) at the level of two fibre tracts, the medial longitudinal fasciculus (mlf) and the lateral longitudinal fasciculus (llf). Other abbreviations: Mi2, Mi3 and Ca, reticulospinal neurons53. Images are dorsal (b, c, e–g, i), ventral (d) and lateral (a, h) views with anterior to the left. Scale bars are 200 μm (a), 50 μm (b–h). Specimen stages: a, c, d (4 dpf), b (2 dpf), e–h (5 dpf).
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f3: Embryonic alignment of precerebellar, pectoral and other hindbrain neurons in transgenic zebrafish.(a) Rhombomere (r) 7–8 YFP expression in hoxb4a enhancer trap line. (b) Reticular (labelled from the spinal cord; red) and YFP (green) neurons showed hindbrain–spinal cord boundary between myotomes (M) 3–4. (c) Half of the pectoral column (labelled from fin bud; red) was within the hindbrain. (d) Occipital motor column (labelled from M1–3/occipital) extended to mid r8, one segment rostral to pectoral motoneurons. (e–g) Dorsal composites (e) and selected confocal planes (f, g) of pectoral (labelled from fin buds; red), inferior olive (IO) and Area II (AII) (labelled from the cerebellum; magenta) neurons in islet-GFP background (green), showing the relative position of pectoral motoneurons with major neuronal subgroups. GFP in this line is expressed in all hindbrain motoneurons, except abducens and pectoral. (h) Vagal (X) and more ventral occipital (Oc) motor columns that extended from spinal cord into the hindbrain (also see f, g). (i) Alignment of pectoral motoneurons (Pec) with other neuronal and anatomical landmarks. Pectoral motoneurons in zebrafish were located across the hindbrain–spinal cord boundary at the level of M3–5 (see Figure 2). Hindbrain motoneurons are located immediately caudal to the inferior olive, below the vagal nucleus (X) and hindbrain commissure (HB com). They are part of the occipital motor column (Oc Mns) at the level of two fibre tracts, the medial longitudinal fasciculus (mlf) and the lateral longitudinal fasciculus (llf). Other abbreviations: Mi2, Mi3 and Ca, reticulospinal neurons53. Images are dorsal (b, c, e–g, i), ventral (d) and lateral (a, h) views with anterior to the left. Scale bars are 200 μm (a), 50 μm (b–h). Specimen stages: a, c, d (4 dpf), b (2 dpf), e–h (5 dpf).

Mentions: We next aligned the pectoral motoneurons with other central nuclei using transgenic zebrafish lines. In the hoxb4a enhancer trap background (Figs 1b and 3a), a gata-2 promotor-driven YFP was inserted 3-kb downstream of the endogenous hoxb4a gene15. Many neurons from rhombomeres (r) 7–8 are genetically labelled with YFP, reflecting the presence of hoxb4a enhancer activity16 (Fig. 3a,b). The retrogradely labelled pectoral motor column was located in posterior r8 and extended into the adjacent spinal cord (Fig. 3c). Notably, the retrogradely labelled occipital motor column extended further rostral than pectoral motoneurons into the middle of r8 (Fig. 3d). Double labelling from the fin and cerebellum in an islet1-GFP transgenic background18 showed the hindbrain pectoral motoneurons to be located immediately caudal to precerebellar neurons (inferior olive/IO and area II/AII) in the middle of r816 (Fig. 3e–g; Supplementary Movie 2). A similar alignment of precerebellar and pectoral neurons in other teleosts studied (midshipman, trout and goldfish; Supplementary Fig. S4) strongly supported a common hindbrain neuronal map for actinopterygians. Occipital and pectoral motoneurons formed a single column (Oc/Pec) that was directly ventral to the posterior half of the vagal (X) motor nucleus in the caudal hindbrain and extended into the anterior spinal cord (Fig. 3h; also see Fig. 2e–h). Neuronal mapping with genetically and retrogradely labelled neurons thus showed pectoral motoneurons distributed across the hindbrain–spinal cord boundary and precisely positioned them with respect to other hindbrain subgroups (summarized in Figure 3i).


Ancestry of motor innervation to pectoral fin and forelimb.

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

Embryonic alignment of precerebellar, pectoral and other hindbrain neurons in transgenic zebrafish.(a) Rhombomere (r) 7–8 YFP expression in hoxb4a enhancer trap line. (b) Reticular (labelled from the spinal cord; red) and YFP (green) neurons showed hindbrain–spinal cord boundary between myotomes (M) 3–4. (c) Half of the pectoral column (labelled from fin bud; red) was within the hindbrain. (d) Occipital motor column (labelled from M1–3/occipital) extended to mid r8, one segment rostral to pectoral motoneurons. (e–g) Dorsal composites (e) and selected confocal planes (f, g) of pectoral (labelled from fin buds; red), inferior olive (IO) and Area II (AII) (labelled from the cerebellum; magenta) neurons in islet-GFP background (green), showing the relative position of pectoral motoneurons with major neuronal subgroups. GFP in this line is expressed in all hindbrain motoneurons, except abducens and pectoral. (h) Vagal (X) and more ventral occipital (Oc) motor columns that extended from spinal cord into the hindbrain (also see f, g). (i) Alignment of pectoral motoneurons (Pec) with other neuronal and anatomical landmarks. Pectoral motoneurons in zebrafish were located across the hindbrain–spinal cord boundary at the level of M3–5 (see Figure 2). Hindbrain motoneurons are located immediately caudal to the inferior olive, below the vagal nucleus (X) and hindbrain commissure (HB com). They are part of the occipital motor column (Oc Mns) at the level of two fibre tracts, the medial longitudinal fasciculus (mlf) and the lateral longitudinal fasciculus (llf). Other abbreviations: Mi2, Mi3 and Ca, reticulospinal neurons53. Images are dorsal (b, c, e–g, i), ventral (d) and lateral (a, h) views with anterior to the left. Scale bars are 200 μm (a), 50 μm (b–h). Specimen stages: a, c, d (4 dpf), b (2 dpf), e–h (5 dpf).
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f3: Embryonic alignment of precerebellar, pectoral and other hindbrain neurons in transgenic zebrafish.(a) Rhombomere (r) 7–8 YFP expression in hoxb4a enhancer trap line. (b) Reticular (labelled from the spinal cord; red) and YFP (green) neurons showed hindbrain–spinal cord boundary between myotomes (M) 3–4. (c) Half of the pectoral column (labelled from fin bud; red) was within the hindbrain. (d) Occipital motor column (labelled from M1–3/occipital) extended to mid r8, one segment rostral to pectoral motoneurons. (e–g) Dorsal composites (e) and selected confocal planes (f, g) of pectoral (labelled from fin buds; red), inferior olive (IO) and Area II (AII) (labelled from the cerebellum; magenta) neurons in islet-GFP background (green), showing the relative position of pectoral motoneurons with major neuronal subgroups. GFP in this line is expressed in all hindbrain motoneurons, except abducens and pectoral. (h) Vagal (X) and more ventral occipital (Oc) motor columns that extended from spinal cord into the hindbrain (also see f, g). (i) Alignment of pectoral motoneurons (Pec) with other neuronal and anatomical landmarks. Pectoral motoneurons in zebrafish were located across the hindbrain–spinal cord boundary at the level of M3–5 (see Figure 2). Hindbrain motoneurons are located immediately caudal to the inferior olive, below the vagal nucleus (X) and hindbrain commissure (HB com). They are part of the occipital motor column (Oc Mns) at the level of two fibre tracts, the medial longitudinal fasciculus (mlf) and the lateral longitudinal fasciculus (llf). Other abbreviations: Mi2, Mi3 and Ca, reticulospinal neurons53. Images are dorsal (b, c, e–g, i), ventral (d) and lateral (a, h) views with anterior to the left. Scale bars are 200 μm (a), 50 μm (b–h). Specimen stages: a, c, d (4 dpf), b (2 dpf), e–h (5 dpf).
Mentions: We next aligned the pectoral motoneurons with other central nuclei using transgenic zebrafish lines. In the hoxb4a enhancer trap background (Figs 1b and 3a), a gata-2 promotor-driven YFP was inserted 3-kb downstream of the endogenous hoxb4a gene15. Many neurons from rhombomeres (r) 7–8 are genetically labelled with YFP, reflecting the presence of hoxb4a enhancer activity16 (Fig. 3a,b). The retrogradely labelled pectoral motor column was located in posterior r8 and extended into the adjacent spinal cord (Fig. 3c). Notably, the retrogradely labelled occipital motor column extended further rostral than pectoral motoneurons into the middle of r8 (Fig. 3d). Double labelling from the fin and cerebellum in an islet1-GFP transgenic background18 showed the hindbrain pectoral motoneurons to be located immediately caudal to precerebellar neurons (inferior olive/IO and area II/AII) in the middle of r816 (Fig. 3e–g; Supplementary Movie 2). A similar alignment of precerebellar and pectoral neurons in other teleosts studied (midshipman, trout and goldfish; Supplementary Fig. S4) strongly supported a common hindbrain neuronal map for actinopterygians. Occipital and pectoral motoneurons formed a single column (Oc/Pec) that was directly ventral to the posterior half of the vagal (X) motor nucleus in the caudal hindbrain and extended into the anterior spinal cord (Fig. 3h; also see Fig. 2e–h). Neuronal mapping with genetically and retrogradely labelled neurons thus showed pectoral motoneurons distributed across the hindbrain–spinal cord boundary and precisely positioned them with respect to other hindbrain subgroups (summarized in Figure 3i).

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
Related in: MedlinePlus