Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion
Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Springer Berlin Heidelberg
2016
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| Online Access: | http://hdl.handle.net/1721.1/105252 https://orcid.org/0000-0002-7644-4498 |
| _version_ | 1811070626135277568 |
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| author | Saltiel, Philippe D'Avella, Andrea Wyler-Duda, Kuno Bizzi, Emilio |
| author2 | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences |
| author_facet | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Saltiel, Philippe D'Avella, Andrea Wyler-Duda, Kuno Bizzi, Emilio |
| author_sort | Saltiel, Philippe |
| collection | MIT |
| description | Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates, with the exception of the interneuronal traveling wave demonstrated in fictive cat scratching (Cuellar et al. J Neurosci 29:798–810, 2009). Here, we reexamine this hypothesis in the frog, using the seven muscle synergies A to G previously identified with intraspinal NMDA (Saltiel et al. J Neurophysiol 85:605–619, 2001). We find that locomotion consists of a sequence of synergy activations (A–B–G–A–F–E–G). The same sequence is observed when focal NMDA iontophoresis in the spinal cord elicits a caudal extension-lateral force-flexion cycle (flexion onset without the C synergy). Examining the early NMDA-evoked motor output at 110 sites reveals a rostrocaudal topographic organization of synergy encoding by the lumbar cord. Each synergy is preferentially activated from distinct regions, which may be multiple, and partially overlap between different synergies. Comparing the sequence of synergy activation in locomotion with their spinal cord topography suggests that the locomotor output is achieved by a rostrocaudally traveling wave of activation in the swing–stance cycle. A two-layer circuitry model, based on this topography and a traveling wave reproduces this output and explores its possible modifications under different afferent inputs. Our results and simulations suggest that a rostrocaudally traveling wave of excitation takes advantage of the topography of interneuronal regions encoding synergies, to activate them in the proper sequence for locomotion. |
| first_indexed | 2024-09-23T08:39:01Z |
| format | Article |
| id | mit-1721.1/105252 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T08:39:01Z |
| publishDate | 2016 |
| publisher | Springer Berlin Heidelberg |
| record_format | dspace |
| spelling | mit-1721.1/1052522022-09-30T10:17:28Z Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion Saltiel, Philippe D'Avella, Andrea Wyler-Duda, Kuno Bizzi, Emilio Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Saltiel, Philippe D'Avella, Andrea Wyler-Duda, Kuno Bizzi, Emilio Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates, with the exception of the interneuronal traveling wave demonstrated in fictive cat scratching (Cuellar et al. J Neurosci 29:798–810, 2009). Here, we reexamine this hypothesis in the frog, using the seven muscle synergies A to G previously identified with intraspinal NMDA (Saltiel et al. J Neurophysiol 85:605–619, 2001). We find that locomotion consists of a sequence of synergy activations (A–B–G–A–F–E–G). The same sequence is observed when focal NMDA iontophoresis in the spinal cord elicits a caudal extension-lateral force-flexion cycle (flexion onset without the C synergy). Examining the early NMDA-evoked motor output at 110 sites reveals a rostrocaudal topographic organization of synergy encoding by the lumbar cord. Each synergy is preferentially activated from distinct regions, which may be multiple, and partially overlap between different synergies. Comparing the sequence of synergy activation in locomotion with their spinal cord topography suggests that the locomotor output is achieved by a rostrocaudally traveling wave of activation in the swing–stance cycle. A two-layer circuitry model, based on this topography and a traveling wave reproduces this output and explores its possible modifications under different afferent inputs. Our results and simulations suggest that a rostrocaudally traveling wave of excitation takes advantage of the topography of interneuronal regions encoding synergies, to activate them in the proper sequence for locomotion. National Institutes of Health (U.S.) (Grant NS 09343) Swiss National Science Foundation 2016-11-07T23:13:37Z 2016-11-07T23:13:37Z 2015-10 2014-12 2016-08-18T15:27:07Z Article http://purl.org/eprint/type/JournalArticle 1863-2653 1863-2661 http://hdl.handle.net/1721.1/105252 Saltiel, Philippe et al. “Synergy Temporal Sequences and Topography in the Spinal Cord: Evidence for a Traveling Wave in Frog Locomotion.” Brain Structure and Function 221.8 (2016): 3869–3890. https://orcid.org/0000-0002-7644-4498 en http://dx.doi.org/10.1007/s00429-015-1133-5 Brain Structure and Function Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/4.0/ Springer-Verlag Berlin Heidelberg application/pdf Springer Berlin Heidelberg Springer Berlin Heidelberg |
| spellingShingle | Saltiel, Philippe D'Avella, Andrea Wyler-Duda, Kuno Bizzi, Emilio Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion |
| title | Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion |
| title_full | Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion |
| title_fullStr | Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion |
| title_full_unstemmed | Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion |
| title_short | Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion |
| title_sort | synergy temporal sequences and topography in the spinal cord evidence for a traveling wave in frog locomotion |
| url | http://hdl.handle.net/1721.1/105252 https://orcid.org/0000-0002-7644-4498 |
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