The Ancient Origins of Neural Substrates for Land Walking

Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated i...

Full description

Saved in:
Bibliographic Details
Published inCell Vol. 172; no. 4; pp. 667 - 682.e15
Main Authors Jung, Heekyung, Baek, Myungin, D’Elia, Kristen P., Boisvert, Catherine, Currie, Peter D., Tay, Boon-Hui, Venkatesh, Byrappa, Brown, Stuart M., Heguy, Adriana, Schoppik, David, Dasen, Jeremy S.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 08.02.2018
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated in primitive marine vertebrates. We show that the neural substrates of bipedalism are present in the little skate Leucoraja erinacea, whose common ancestor with tetrapods existed ∼420 million years ago. Leucoraja exhibits core features of tetrapod locomotor gaits, including left-right alternation and reciprocal extension-flexion of the pelvic fins. Leucoraja also deploys a remarkably conserved Hox transcription factor-dependent program that is essential for selective innervation of fin/limb muscle. This network encodes peripheral connectivity modules that are distinct from those used in axial muscle-based swimming and has apparently been diminished in most modern fish. These findings indicate that the circuits that are essential for walking evolved through adaptation of a genetic regulatory network shared by all vertebrates with paired appendages. [Display omitted] [Display omitted] •The little skate Leucoraja erinacea exhibits bipedal walking-like behaviors•Neuronal subtypes essential for walking originated in primitive jawed fish•Fin and limb motor neurons share a common Hox-dependent gene network•Modulation of Hox patterning facilitates evolutionary changes in MN organization The circuits involved in limb control were established in the common ancestor to all vertebrates with pair appendages millions of years before the first tetrapod walked on land.
AbstractList Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated in primitive marine vertebrates. We show that the neural substrates of bipedalism are present in the little skate Leucoraja erinacea , whose common ancestor with tetrapods existed ~420 million years ago. Leucoraja exhibits core features of tetrapod locomotor gaits, including left-right alternation and reciprocal extension-flexion of the pelvic fins. Leucoraja also deploys a remarkably conserved Hox transcription factor-dependent program essential for selective innervation of fin/limb muscle. This network encodes peripheral connectivity modules distinct from those used in axial muscle-based swimming, and has been apparently diminished in most modern fish. These findings indicate that the circuits essential for walking evolved through adaptation of a genetic regulatory network shared by all vertebrates with paired appendages. The circuits involved in limb control were established in the common ancestor to all vertebrates with pair appendages millions of years before the first tetrapod walked on land
Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated in primitive marine vertebrates. We show that the neural substrates of bipedalism are present in the little skate Leucoraja erinacea, whose common ancestor with tetrapods existed ∼420 million years ago. Leucoraja exhibits core features of tetrapod locomotor gaits, including left-right alternation and reciprocal extension-flexion of the pelvic fins. Leucoraja also deploys a remarkably conserved Hox transcription factor-dependent program that is essential for selective innervation of fin/limb muscle. This network encodes peripheral connectivity modules that are distinct from those used in axial muscle-based swimming and has apparently been diminished in most modern fish. These findings indicate that the circuits that are essential for walking evolved through adaptation of a genetic regulatory network shared by all vertebrates with paired appendages. VIDEO ABSTRACT.
Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated in primitive marine vertebrates. We show that the neural substrates of bipedalism are present in the little skate Leucoraja erinacea, whose common ancestor with tetrapods existed ∼420 million years ago. Leucoraja exhibits core features of tetrapod locomotor gaits, including left-right alternation and reciprocal extension-flexion of the pelvic fins. Leucoraja also deploys a remarkably conserved Hox transcription factor-dependent program that is essential for selective innervation of fin/limb muscle. This network encodes peripheral connectivity modules that are distinct from those used in axial muscle-based swimming and has apparently been diminished in most modern fish. These findings indicate that the circuits that are essential for walking evolved through adaptation of a genetic regulatory network shared by all vertebrates with paired appendages. [Display omitted] [Display omitted] •The little skate Leucoraja erinacea exhibits bipedal walking-like behaviors•Neuronal subtypes essential for walking originated in primitive jawed fish•Fin and limb motor neurons share a common Hox-dependent gene network•Modulation of Hox patterning facilitates evolutionary changes in MN organization The circuits involved in limb control were established in the common ancestor to all vertebrates with pair appendages millions of years before the first tetrapod walked on land.
Author Venkatesh, Byrappa
Brown, Stuart M.
Dasen, Jeremy S.
Jung, Heekyung
Baek, Myungin
Schoppik, David
Boisvert, Catherine
D’Elia, Kristen P.
Tay, Boon-Hui
Heguy, Adriana
Currie, Peter D.
AuthorAffiliation 4 EMBL Australia, Melbourne Node, Monash University, Clayton, VIC 3800, Australia
3 Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, VIC 3800, Australia
6 Department of Pediatrics, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228
1 Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
8 Genome technology Center, Division for Advanced Research Technologies, and Department of Pathology, NYU School of Medicine, New York, NY 10016, USA
5 Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Biopolis, Singapore 138673
2 Department of Environment and Agriculture, Curtin University, Bentley, WA, 6102, Australia
9 Department of Otolaryngology, NYU School of Medicine, New York, NY 10016, USA
7 Applied Bioinformatics Laboratory, NYU School of Medicine, New York, NY 10016 USA
AuthorAffiliation_xml – name: 8 Genome technology Center, Division for Advanced Research Technologies, and Department of Pathology, NYU School of Medicine, New York, NY 10016, USA
– name: 7 Applied Bioinformatics Laboratory, NYU School of Medicine, New York, NY 10016 USA
– name: 1 Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
– name: 6 Department of Pediatrics, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 119228
– name: 4 EMBL Australia, Melbourne Node, Monash University, Clayton, VIC 3800, Australia
– name: 5 Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Biopolis, Singapore 138673
– name: 2 Department of Environment and Agriculture, Curtin University, Bentley, WA, 6102, Australia
– name: 9 Department of Otolaryngology, NYU School of Medicine, New York, NY 10016, USA
– name: 3 Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, VIC 3800, Australia
Author_xml – sequence: 1
  givenname: Heekyung
  surname: Jung
  fullname: Jung, Heekyung
  organization: Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
– sequence: 2
  givenname: Myungin
  surname: Baek
  fullname: Baek, Myungin
  organization: Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
– sequence: 3
  givenname: Kristen P.
  surname: D’Elia
  fullname: D’Elia, Kristen P.
  organization: Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
– sequence: 4
  givenname: Catherine
  surname: Boisvert
  fullname: Boisvert, Catherine
  organization: Department of Environment and Agriculture, Curtin University, Bentley, WA 6102, Australia
– sequence: 5
  givenname: Peter D.
  surname: Currie
  fullname: Currie, Peter D.
  organization: Australian Regenerative Medicine Institute (ARMI), Monash University, Clayton, VIC 3800, Australia
– sequence: 6
  givenname: Boon-Hui
  surname: Tay
  fullname: Tay, Boon-Hui
  organization: Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Biopolis, Singapore 138673, Singapore
– sequence: 7
  givenname: Byrappa
  surname: Venkatesh
  fullname: Venkatesh, Byrappa
  organization: Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Biopolis, Singapore 138673, Singapore
– sequence: 8
  givenname: Stuart M.
  surname: Brown
  fullname: Brown, Stuart M.
  organization: Applied Bioinformatics Laboratory, NYU School of Medicine, New York, NY 10016, USA
– sequence: 9
  givenname: Adriana
  surname: Heguy
  fullname: Heguy, Adriana
  organization: Genome Technology Center, Division for Advanced Research Technologies, and Department of Pathology, NYU School of Medicine, New York, NY 10016, USA
– sequence: 10
  givenname: David
  surname: Schoppik
  fullname: Schoppik, David
  organization: Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
– sequence: 11
  givenname: Jeremy S.
  surname: Dasen
  fullname: Dasen, Jeremy S.
  email: jeremy.dasen@nyumc.org
  organization: Neuroscience Institute, Department of Neuroscience and Physiology, NYU School of Medicine, New York, NY 10016, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29425489$$D View this record in MEDLINE/PubMed
BookMark eNp9kE9P3DAQxS0EKgvtF-ihyrGXLGPHjhMJISFU_kgrOADq0XLsyeJt1qZ2gsS3r6MF1F4qjeSD33vz5ndE9n3wSMhXCksKtD7ZLA0Ow5IBbZZA81R7ZEGhlSWnku2TBUDLyqaW_JAcpbQBgEYI8YkcspYzwZt2QdqHJyzOvXHox-IuurXzqQh9cYtT1ENxP3VpjHrEVPQhFivtbfFTD7-cX38mB70eEn55e4_J4-WPh4vrcnV3dXNxviqNYHQsbS-sYLzWjWBdJ2kvOa1YQ9veANLKInIJUFWaGwsGOtFxbShH3duGQb7pmJztcp-nbovW5KK5mXqObqvjqwraqX9_vHtS6_CiRJPPlTIHfH8LiOH3hGlUW5dmctpjmJKat0AtaQ1ZynZSE0NKEfuPNRTUzFxt1OxUM3MFNE-VTd_-LvhheYecBac7AWZMLw6jSjNvg9ZFNKOywf0v_w_Yd5RQ
CitedBy_id crossref_primary_10_3389_fncir_2023_1146449
crossref_primary_10_1016_j_conb_2023_102753
crossref_primary_10_1111_dgd_12824
crossref_primary_10_3390_fishes8050271
crossref_primary_10_1111_1468_5922_12642
crossref_primary_10_1016_j_anbehav_2019_06_013
crossref_primary_10_1111_jfb_15165
crossref_primary_10_1016_j_semcdb_2023_03_014
crossref_primary_10_1016_j_tins_2018_07_013
crossref_primary_10_7554_eLife_45839
crossref_primary_10_1016_j_tins_2020_08_006
crossref_primary_10_1242_dev_194761
crossref_primary_10_1038_d41586_023_00192_0
crossref_primary_10_1152_physrev_00015_2019
crossref_primary_10_3389_fnins_2021_686481
crossref_primary_10_1016_j_conb_2018_04_012
crossref_primary_10_1038_d41586_018_01700_3
crossref_primary_10_3389_fnins_2022_854422
crossref_primary_10_1016_j_isci_2022_104083
crossref_primary_10_1016_j_ydbio_2021_06_001
crossref_primary_10_1016_j_conb_2021_07_015
crossref_primary_10_3389_fevo_2021_679633
crossref_primary_10_1016_j_conb_2021_07_016
crossref_primary_10_1016_j_celrep_2019_04_113
crossref_primary_10_1093_iob_obac042
crossref_primary_10_3390_life11020136
crossref_primary_10_1186_s13064_018_0108_7
crossref_primary_10_1186_s40851_018_0110_2
crossref_primary_10_1098_rspb_2019_1571
crossref_primary_10_3389_fmars_2022_831926
crossref_primary_10_1016_j_dsr_2019_103104
crossref_primary_10_1093_icb_icac095
crossref_primary_10_1016_j_conb_2018_04_024
crossref_primary_10_1371_journal_pone_0265469
crossref_primary_10_1038_s41467_022_35574_x
crossref_primary_10_1038_s41597_024_03514_7
crossref_primary_10_1017_S1755691018000695
crossref_primary_10_1002_dneu_22799
crossref_primary_10_1088_1748_3190_aada54
crossref_primary_10_1038_s41593_023_01479_1
crossref_primary_10_1111_1468_5922_12821
crossref_primary_10_3389_fnbot_2022_883641
crossref_primary_10_1038_s41583_019_0168_7
crossref_primary_10_1038_s41583_021_00497_x
crossref_primary_10_1007_s11160_022_09706_x
crossref_primary_10_7554_eLife_78345
crossref_primary_10_1098_rspb_2021_0937
crossref_primary_10_1146_annurev_neuro_083122_025325
crossref_primary_10_1098_rsbl_2018_0647
crossref_primary_10_1016_j_cophys_2019_02_003
crossref_primary_10_1523_ENEURO_0226_23_2023
crossref_primary_10_1038_d41586_018_07684_4
crossref_primary_10_1016_j_cub_2023_11_062
crossref_primary_10_1016_j_celrep_2023_113049
crossref_primary_10_1111_dgd_12670
Cites_doi 10.1016/j.cell.2008.06.019
10.1038/nprot.2013.084
10.1016/j.cell.2015.06.036
10.1016/j.neuron.2012.05.011
10.1186/1471-2148-9-218
10.1242/jeb.204.2.379
10.1002/jmor.10865
10.1016/j.neuron.2006.11.008
10.1002/dneu.20589
10.1016/j.neuron.2008.06.025
10.1016/j.neuron.2014.11.024
10.1126/science.1245629
10.1038/ncomms1045
10.1016/j.neuron.2015.08.005
10.1643/CG-02-153R1
10.1016/j.devcel.2015.01.008
10.1098/rstb.1993.0007
10.1038/nature13708
10.1093/bioinformatics/btp616
10.1242/dev.121.12.4117
10.1016/j.neuron.2014.02.013
10.1038/nature05436
10.1016/j.cell.2011.10.012
10.1371/journal.pgen.1004245
10.1111/j.1525-142X.2012.00561.x
10.1016/j.conb.2009.10.011
10.1016/j.ydbio.2011.04.009
10.1371/journal.pbio.1001773
10.1038/nature19322
10.1002/ar.20719
10.1126/science.1210912
10.1016/j.neuron.2010.08.008
10.1016/S0896-6273(01)00544-X
10.1016/S0092-8674(00)81783-3
10.1016/j.devcel.2014.03.008
10.1016/j.semcdb.2011.10.016
10.1073/pnas.1118669109
10.1093/bioinformatics/btu170
10.1038/nature16497
10.1073/pnas.1521818112
10.1159/000113905
10.1016/j.cell.2005.09.009
10.1038/nprot.2007.416
10.1016/j.brainresrev.2007.07.006
10.1002/dvg.20597
10.1242/dev.02044
10.1016/j.neuron.2013.09.020
10.1371/journal.pgen.1003184
10.1046/j.1095-8312.2002.00085.x
10.12688/f1000research.4996.1
10.1016/j.celrep.2017.10.004
10.1038/nmeth.4197
10.1038/srep23711
10.1016/0092-8674(94)90027-2
ContentType Journal Article
Copyright 2018 Elsevier Inc.
Copyright © 2018 Elsevier Inc. All rights reserved.
Copyright_xml – notice: 2018 Elsevier Inc.
– notice: Copyright © 2018 Elsevier Inc. All rights reserved.
DBID 6I.
AAFTH
CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
5PM
DOI 10.1016/j.cell.2018.01.013
DatabaseName ScienceDirect Open Access Titles
Elsevier:ScienceDirect:Open Access
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
MEDLINE - Academic
DatabaseTitleList
MEDLINE

Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
EISSN 1097-4172
EndPage 682.e15
ExternalDocumentID 10_1016_j_cell_2018_01_013
29425489
S0092867418300503
Genre Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIMH NIH HHS
  grantid: T32 MH096331
– fundername: NINDS NIH HHS
  grantid: R01 NS062822
– fundername: NINDS NIH HHS
  grantid: R21 NS099933
– fundername: Howard Hughes Medical Institute
GroupedDBID ---
--K
-DZ
-ET
-~X
0R~
0WA
1RT
1~5
29B
2FS
2WC
3EH
4.4
457
4G.
53G
5GY
5RE
62-
6I.
6J9
7-5
85S
AACTN
AAEDW
AAFTH
AAFWJ
AAIAV
AAKRW
AAKUH
AALRI
AAUCE
AAVLU
AAXJY
AAXUO
ABCQX
ABJNI
ABMAC
ABMWF
ABOCM
ABVKL
ACGFO
ACGFS
ACNCT
ADBBV
ADEZE
ADJPV
AEFWE
AENEX
AEXQZ
AFTJW
AGHSJ
AGKMS
AHHHB
AITUG
ALKID
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
ASPBG
AVWKF
AZFZN
BAWUL
CS3
DIK
DU5
E3Z
EBS
EJD
F5P
FCP
FDB
FIRID
HH5
IH2
IHE
IXB
J1W
JIG
K-O
KOO
KQ8
L7B
LX5
M3Z
M41
N9A
NCXOZ
O-L
O9-
OK1
P2P
RCE
RIG
RNS
ROL
RPZ
SCP
SDG
SDP
SES
SSZ
TAE
TN5
TR2
TWZ
UKR
UPT
VQA
WH7
WQ6
YZZ
ZA5
ZCA
0SF
AAEDT
AAHBH
AAMRU
ADVLN
AKAPO
AKRWK
CGR
CUY
CVF
ECM
EIF
NPM
.-4
.55
.GJ
.HR
1CY
1VV
2KS
3O-
5VS
6TJ
9M8
AAIKJ
AAQFI
AAQXK
AAYJJ
AAYXX
ABDPE
ABEFU
ABTAH
ACRPL
ADMUD
ADNMO
AGHFR
AI.
AIDAL
CITATION
FEDTE
FGOYB
G-2
HVGLF
HZ~
H~9
MVM
OHT
OMK
OZT
PUQ
R2-
UBW
UHB
VH1
X7M
YYP
YYQ
ZGI
ZHY
ZKB
ZY4
7X8
5PM
ID FETCH-LOGICAL-c521t-df5d5246a852bb71f74132819fc0e13dee470033a4cd0c0b5b4ac14eafd820013
IEDL.DBID ABVKL
ISSN 0092-8674
IngestDate Tue Sep 17 21:15:28 EDT 2024
Sun Sep 29 07:18:15 EDT 2024
Fri Dec 06 02:39:28 EST 2024
Sat Nov 02 12:22:47 EDT 2024
Fri Feb 23 02:47:53 EST 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 4
Keywords neural circuit
development
Hox gene
motor neuron
locomotion
spinal cord
evolution
Language English
License This article is made available under the Elsevier license.
Copyright © 2018 Elsevier Inc. All rights reserved.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c521t-df5d5246a852bb71f74132819fc0e13dee470033a4cd0c0b5b4ac14eafd820013
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Equal contribution
OpenAccessLink https://www.sciencedirect.com/science/article/pii/S0092867418300503
PMID 29425489
PQID 2001067160
PQPubID 23479
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_5808577
proquest_miscellaneous_2001067160
crossref_primary_10_1016_j_cell_2018_01_013
pubmed_primary_29425489
elsevier_sciencedirect_doi_10_1016_j_cell_2018_01_013
PublicationCentury 2000
PublicationDate 2018-02-08
PublicationDateYYYYMMDD 2018-02-08
PublicationDate_xml – month: 02
  year: 2018
  text: 2018-02-08
  day: 08
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Cell
PublicationTitleAlternate Cell
PublicationYear 2018
Publisher Elsevier Inc
Publisher_xml – name: Elsevier Inc
References Tanabe, William, Jessell (bib49) 1998; 95
Nishimoto, Minguillon, Wood, Logan (bib40) 2014; 10
Dasen, Tice, Brenner-Morton, Jessell (bib8) 2005; 123
Dahn, Davis, Pappano, Shubin (bib7) 2007; 445
Haas, Papanicolaou, Yassour, Grabherr, Blood, Bowden, Couger, Eccles, Li, Lieber (bib18) 2013; 8
Rousso, Gaber, Wellik, Morrisey, Novitch (bib45) 2008; 59
Koester, Spirito (bib28) 2003; 2003
Hinckley, Alaynick, Gallarda, Hayashi, Hilde, Driscoll, Dekker, Tucker, Sharpee, Pfaff (bib20) 2015; 87
Standen, Du, Larsson (bib47) 2014; 513
Grillner, Jessell (bib17) 2009; 19
Hempel, Sugino, Nelson (bib19) 2007; 2
Kao, Law, Kania (bib25) 2012; 23
Fetcho (bib11) 1992; 40
Machado, Pnevmatikakis, Paninski, Jessell, Miri (bib34) 2015; 162
Robinson, McCarthy, Smyth (bib43) 2010; 26
Tsuchida, Ensini, Morton, Baldassare, Edlund, Jessell, Pfaff (bib51) 1994; 79
Gillis, Shubin (bib14) 2009; 47
Grillner (bib16) 2006; 52
Ma, Gilland, Bass, Baker (bib32) 2010; 1
Macesic, Kajiura (bib33) 2010; 271
Holst, Bone (bib21) 1993; 339
Maxwell, Fröbisch, Heppleston (bib35) 2008; 291
Flanagan-Steet, Fox, Meyer, Sanes (bib13) 2005; 132
Woltering, Noordermeer, Leleu, Duboule (bib52) 2014; 12
Lacombe, Hanley, Jung, Philippidou, Surmeli, Grinstein, Dasen (bib29) 2013; 9
Flammang, Suvarnaraksha, Markiewicz, Soares (bib12) 2016; 6
Dasen, De Camilli, Wang, Tucker, Jessell (bib9) 2008; 134
Bolger, Lohse, Usadel (bib5) 2014; 30
Jung, Mazzoni, Soshnikova, Hanley, Venkatesh, Duboule, Dasen (bib24) 2014; 29
Arber (bib2) 2012; 74
Bagnall, McLean (bib4) 2014; 343
King, Gillis, Carlisle, Dahn (bib26) 2011; 334
Nakamura, Gehrke, Lemberg, Szymaszek, Shubin (bib39) 2016; 537
Nakamura, Klomp, Pieretti, Schneider, Gehrke, Shubin (bib38) 2015; 112
Lucifora, Vassallo (bib31) 2002; 77
Murakami, Tanaka (bib37) 2011; 355
Dixit, Vijayraghavan, Bate (bib10) 2008; 68
Sürmeli, Akay, Ippolito, Tucker, Jessell (bib48) 2011; 147
Liu, Laufer, Jessell (bib30) 2001; 32
Jung, Dasen (bib22) 2015; 32
Patro, Duggal, Love, Irizarry, Kingsford (bib41) 2017; 14
Chevallier, Jan Ijspeert, Ryczko, Nagy, Cabelguen (bib6) 2008; 57
King, Shubin, Coates, Hale (bib27) 2011; 108
Zhang, Lanuza, Britz, Wang, Siembab, Zhang, Velasquez, Alvarez, Frank, Goulding (bib54) 2014; 82
Appel, Korzh, Glasgow, Thor, Edlund, Dawid, Eisen (bib1) 1995; 121
Jung, Lacombe, Mazzoni, Liem, Grinstein, Mahony, Mukhopadhyay, Gifford, Young, Anderson (bib23) 2010; 67
Tanaka, Onimaru (bib50) 2012; 14
Baek, Pivetta, Liu, Arber, Dasen (bib3) 2017; 21
Goetz, Pivetta, Arber (bib15) 2015; 85
Philippidou, Dasen (bib42) 2013; 80
Mulley, Zhong, Holland (bib36) 2009; 9
Song, Ampatzis, Björnfors, El Manira (bib46) 2016; 529
Rosenberger (bib44) 2001; 204
Wyffels, King, Vincent, Chen, Wu, Polson (bib53) 2014; 3
Jung (10.1016/j.cell.2018.01.013_bib22) 2015; 32
Jung (10.1016/j.cell.2018.01.013_bib23) 2010; 67
Lacombe (10.1016/j.cell.2018.01.013_bib29) 2013; 9
Liu (10.1016/j.cell.2018.01.013_bib30) 2001; 32
Sürmeli (10.1016/j.cell.2018.01.013_bib48) 2011; 147
Mulley (10.1016/j.cell.2018.01.013_bib36) 2009; 9
Dahn (10.1016/j.cell.2018.01.013_bib7) 2007; 445
Gillis (10.1016/j.cell.2018.01.013_bib14) 2009; 47
Bagnall (10.1016/j.cell.2018.01.013_bib4) 2014; 343
Tanabe (10.1016/j.cell.2018.01.013_bib49) 1998; 95
Maxwell (10.1016/j.cell.2018.01.013_bib35) 2008; 291
Dasen (10.1016/j.cell.2018.01.013_bib8) 2005; 123
Standen (10.1016/j.cell.2018.01.013_bib47) 2014; 513
Baek (10.1016/j.cell.2018.01.013_bib3) 2017; 21
Kao (10.1016/j.cell.2018.01.013_bib25) 2012; 23
Nakamura (10.1016/j.cell.2018.01.013_bib38) 2015; 112
King (10.1016/j.cell.2018.01.013_bib26) 2011; 334
Tsuchida (10.1016/j.cell.2018.01.013_bib51) 1994; 79
Chevallier (10.1016/j.cell.2018.01.013_bib6) 2008; 57
Nishimoto (10.1016/j.cell.2018.01.013_bib40) 2014; 10
Haas (10.1016/j.cell.2018.01.013_bib18) 2013; 8
Machado (10.1016/j.cell.2018.01.013_bib34) 2015; 162
Flammang (10.1016/j.cell.2018.01.013_bib12) 2016; 6
Grillner (10.1016/j.cell.2018.01.013_bib17) 2009; 19
Tanaka (10.1016/j.cell.2018.01.013_bib50) 2012; 14
Hinckley (10.1016/j.cell.2018.01.013_bib20) 2015; 87
Lucifora (10.1016/j.cell.2018.01.013_bib31) 2002; 77
Song (10.1016/j.cell.2018.01.013_bib46) 2016; 529
Dasen (10.1016/j.cell.2018.01.013_bib9) 2008; 134
Hempel (10.1016/j.cell.2018.01.013_bib19) 2007; 2
Ma (10.1016/j.cell.2018.01.013_bib32) 2010; 1
Rosenberger (10.1016/j.cell.2018.01.013_bib44) 2001; 204
Appel (10.1016/j.cell.2018.01.013_bib1) 1995; 121
Zhang (10.1016/j.cell.2018.01.013_bib54) 2014; 82
Bolger (10.1016/j.cell.2018.01.013_bib5) 2014; 30
Koester (10.1016/j.cell.2018.01.013_bib28) 2003; 2003
Robinson (10.1016/j.cell.2018.01.013_bib43) 2010; 26
Arber (10.1016/j.cell.2018.01.013_bib2) 2012; 74
Flanagan-Steet (10.1016/j.cell.2018.01.013_bib13) 2005; 132
Goetz (10.1016/j.cell.2018.01.013_bib15) 2015; 85
Holst (10.1016/j.cell.2018.01.013_bib21) 1993; 339
Macesic (10.1016/j.cell.2018.01.013_bib33) 2010; 271
Rousso (10.1016/j.cell.2018.01.013_bib45) 2008; 59
Wyffels (10.1016/j.cell.2018.01.013_bib53) 2014; 3
Woltering (10.1016/j.cell.2018.01.013_bib52) 2014; 12
Murakami (10.1016/j.cell.2018.01.013_bib37) 2011; 355
Fetcho (10.1016/j.cell.2018.01.013_bib11) 1992; 40
Patro (10.1016/j.cell.2018.01.013_bib41) 2017; 14
Jung (10.1016/j.cell.2018.01.013_bib24) 2014; 29
Nakamura (10.1016/j.cell.2018.01.013_bib39) 2016; 537
Grillner (10.1016/j.cell.2018.01.013_bib16) 2006; 52
Philippidou (10.1016/j.cell.2018.01.013_bib42) 2013; 80
King (10.1016/j.cell.2018.01.013_bib27) 2011; 108
Dixit (10.1016/j.cell.2018.01.013_bib10) 2008; 68
References_xml – volume: 87
  start-page: 1008
  year: 2015
  end-page: 1021
  ident: bib20
  article-title: Spinal Locomotor Circuits Develop Using Hierarchical Rules Based on Motorneuron Position and Identity
  publication-title: Neuron
  contributor:
    fullname: Pfaff
– volume: 291
  start-page: 1079
  year: 2008
  end-page: 1087
  ident: bib35
  article-title: Variability and conservation in late chondrichthyan development: ontogeny of the winter skate (Leucoraja ocellata)
  publication-title: Anat. Rec. (Hoboken)
  contributor:
    fullname: Heppleston
– volume: 40
  start-page: 82
  year: 1992
  end-page: 97
  ident: bib11
  article-title: The spinal motor system in early vertebrates and some of its evolutionary changes
  publication-title: Brain Behav. Evol.
  contributor:
    fullname: Fetcho
– volume: 32
  start-page: 408
  year: 2015
  end-page: 422
  ident: bib22
  article-title: Evolution of patterning systems and circuit elements for locomotion
  publication-title: Dev. Cell
  contributor:
    fullname: Dasen
– volume: 59
  start-page: 226
  year: 2008
  end-page: 240
  ident: bib45
  article-title: Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons
  publication-title: Neuron
  contributor:
    fullname: Novitch
– volume: 79
  start-page: 957
  year: 1994
  end-page: 970
  ident: bib51
  article-title: Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes
  publication-title: Cell
  contributor:
    fullname: Pfaff
– volume: 6
  start-page: 23711
  year: 2016
  ident: bib12
  article-title: Tetrapod-like pelvic girdle in a walking cavefish
  publication-title: Sci. Rep.
  contributor:
    fullname: Soares
– volume: 82
  start-page: 138
  year: 2014
  end-page: 150
  ident: bib54
  article-title: V1 and v2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion
  publication-title: Neuron
  contributor:
    fullname: Goulding
– volume: 121
  start-page: 4117
  year: 1995
  end-page: 4125
  ident: bib1
  article-title: Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish
  publication-title: Development
  contributor:
    fullname: Eisen
– volume: 67
  start-page: 781
  year: 2010
  end-page: 796
  ident: bib23
  article-title: Global control of motor neuron topography mediated by the repressive actions of a single hox gene
  publication-title: Neuron
  contributor:
    fullname: Anderson
– volume: 343
  start-page: 197
  year: 2014
  end-page: 200
  ident: bib4
  article-title: Modular organization of axial microcircuits in zebrafish
  publication-title: Science
  contributor:
    fullname: McLean
– volume: 9
  start-page: 218
  year: 2009
  ident: bib36
  article-title: Comparative genomics of chondrichthyan Hoxa clusters
  publication-title: BMC Evol. Biol.
  contributor:
    fullname: Holland
– volume: 80
  start-page: 12
  year: 2013
  end-page: 34
  ident: bib42
  article-title: Hox genes: choreographers in neural development, architects of circuit organization
  publication-title: Neuron
  contributor:
    fullname: Dasen
– volume: 23
  start-page: 83
  year: 2012
  end-page: 91
  ident: bib25
  article-title: Eph and ephrin signaling: lessons learned from spinal motor neurons
  publication-title: Semin. Cell Dev. Biol.
  contributor:
    fullname: Kania
– volume: 30
  start-page: 2114
  year: 2014
  end-page: 2120
  ident: bib5
  article-title: Trimmomatic: a flexible trimmer for Illumina sequence data
  publication-title: Bioinformatics
  contributor:
    fullname: Usadel
– volume: 513
  start-page: 54
  year: 2014
  end-page: 58
  ident: bib47
  article-title: Developmental plasticity and the origin of tetrapods
  publication-title: Nature
  contributor:
    fullname: Larsson
– volume: 8
  start-page: 1494
  year: 2013
  end-page: 1512
  ident: bib18
  article-title: De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis
  publication-title: Nat. Protoc.
  contributor:
    fullname: Lieber
– volume: 21
  start-page: 867
  year: 2017
  end-page: 877
  ident: bib3
  article-title: Columnar-Intrinsic Cues Shape Premotor Input Specificity in Locomotor Circuits
  publication-title: Cell Rep.
  contributor:
    fullname: Dasen
– volume: 9
  start-page: e1003184
  year: 2013
  ident: bib29
  article-title: Genetic and functional modularity of Hox activities in the specification of limb-innervating motor neurons
  publication-title: PLoS Genet.
  contributor:
    fullname: Dasen
– volume: 537
  start-page: 225
  year: 2016
  end-page: 228
  ident: bib39
  article-title: Digits and fin rays share common developmental histories
  publication-title: Nature
  contributor:
    fullname: Shubin
– volume: 68
  start-page: 309
  year: 2008
  end-page: 316
  ident: bib10
  article-title: Hox genes and the regulation of movement in Drosophila
  publication-title: Dev. Neurobiol.
  contributor:
    fullname: Bate
– volume: 529
  start-page: 399
  year: 2016
  end-page: 402
  ident: bib46
  article-title: Motor neurons control locomotor circuit function retrogradely via gap junctions
  publication-title: Nature
  contributor:
    fullname: El Manira
– volume: 77
  start-page: 35
  year: 2002
  end-page: 41
  ident: bib31
  article-title: Walking in skates (Chondrichthyes, Rajidae): anatomy, behaviour and analogies to tetrapod locomotion
  publication-title: Biol. J. Linn. Soc. Lond.
  contributor:
    fullname: Vassallo
– volume: 52
  start-page: 751
  year: 2006
  end-page: 766
  ident: bib16
  article-title: Biological pattern generation: the cellular and computational logic of networks in motion
  publication-title: Neuron
  contributor:
    fullname: Grillner
– volume: 2003
  start-page: 553
  year: 2003
  end-page: 561
  ident: bib28
  article-title: Punting: An unusual mode of locomotion in the little skate, Leucoraja erinacea (Chondrichthyes: Rajidae)
  publication-title: Copeia
  contributor:
    fullname: Spirito
– volume: 204
  start-page: 379
  year: 2001
  end-page: 394
  ident: bib44
  article-title: Pectoral fin locomotion in batoid fishes: undulation versus oscillation
  publication-title: J. Exp. Biol.
  contributor:
    fullname: Rosenberger
– volume: 2
  start-page: 2924
  year: 2007
  end-page: 2929
  ident: bib19
  article-title: A manual method for the purification of fluorescently labeled neurons from the mammalian brain
  publication-title: Nat. Protoc.
  contributor:
    fullname: Nelson
– volume: 10
  start-page: e1004245
  year: 2014
  ident: bib40
  article-title: A combination of activation and repression by a colinear Hox code controls forelimb-restricted expression of Tbx5 and reveals Hox protein specificity
  publication-title: PLoS Genet.
  contributor:
    fullname: Logan
– volume: 26
  start-page: 139
  year: 2010
  end-page: 140
  ident: bib43
  article-title: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
  publication-title: Bioinformatics
  contributor:
    fullname: Smyth
– volume: 355
  start-page: 164
  year: 2011
  end-page: 172
  ident: bib37
  article-title: Evolution of motor innervation to vertebrate fins and limbs
  publication-title: Dev. Biol.
  contributor:
    fullname: Tanaka
– volume: 123
  start-page: 477
  year: 2005
  end-page: 491
  ident: bib8
  article-title: A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity
  publication-title: Cell
  contributor:
    fullname: Jessell
– volume: 108
  start-page: 21146
  year: 2011
  end-page: 21151
  ident: bib27
  article-title: Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes
  publication-title: Proc. Natl. Acad. Sci. USA
  contributor:
    fullname: Hale
– volume: 14
  start-page: 412
  year: 2012
  end-page: 420
  ident: bib50
  article-title: Acquisition of the paired fins: a view from the sequential evolution of the lateral plate mesoderm
  publication-title: Evol. Dev.
  contributor:
    fullname: Onimaru
– volume: 162
  start-page: 338
  year: 2015
  end-page: 350
  ident: bib34
  article-title: Primacy of Flexor Locomotor Pattern Revealed by Ancestral Reversion of Motor Neuron Identity
  publication-title: Cell
  contributor:
    fullname: Miri
– volume: 32
  start-page: 997
  year: 2001
  end-page: 1012
  ident: bib30
  article-title: Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids
  publication-title: Neuron
  contributor:
    fullname: Jessell
– volume: 334
  start-page: 1517
  year: 2011
  ident: bib26
  article-title: A natural deletion of the HoxC cluster in elasmobranch fishes
  publication-title: Science
  contributor:
    fullname: Dahn
– volume: 12
  start-page: e1001773
  year: 2014
  ident: bib52
  article-title: Conservation and divergence of regulatory strategies at Hox Loci and the origin of tetrapod digits
  publication-title: PLoS Biol.
  contributor:
    fullname: Duboule
– volume: 132
  start-page: 4471
  year: 2005
  end-page: 4481
  ident: bib13
  article-title: Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations
  publication-title: Development
  contributor:
    fullname: Sanes
– volume: 19
  start-page: 572
  year: 2009
  end-page: 586
  ident: bib17
  article-title: Measured motion: searching for simplicity in spinal locomotor networks
  publication-title: Curr. Opin. Neurobiol.
  contributor:
    fullname: Jessell
– volume: 1
  start-page: 49
  year: 2010
  ident: bib32
  article-title: Ancestry of motor innervation to pectoral fin and forelimb
  publication-title: Nat. Commun.
  contributor:
    fullname: Baker
– volume: 74
  start-page: 975
  year: 2012
  end-page: 989
  ident: bib2
  article-title: Motor circuits in action: specification, connectivity, and function
  publication-title: Neuron
  contributor:
    fullname: Arber
– volume: 112
  start-page: 15940
  year: 2015
  end-page: 15945
  ident: bib38
  article-title: Molecular mechanisms underlying the exceptional adaptations of batoid fins
  publication-title: Proc. Natl. Acad. Sci. USA
  contributor:
    fullname: Shubin
– volume: 29
  start-page: 171
  year: 2014
  end-page: 187
  ident: bib24
  article-title: Evolving Hox activity profiles govern diversity in locomotor systems
  publication-title: Dev. Cell
  contributor:
    fullname: Dasen
– volume: 271
  start-page: 1219
  year: 2010
  end-page: 1228
  ident: bib33
  article-title: Comparative punting kinematics and pelvic fin musculature of benthic batoids
  publication-title: J. Morphol.
  contributor:
    fullname: Kajiura
– volume: 14
  start-page: 417
  year: 2017
  end-page: 419
  ident: bib41
  article-title: Salmon provides fast and bias-aware quantification of transcript expression
  publication-title: Nat. Methods
  contributor:
    fullname: Kingsford
– volume: 95
  start-page: 67
  year: 1998
  end-page: 80
  ident: bib49
  article-title: Specification of motor neuron identity by the MNR2 homeodomain protein
  publication-title: Cell
  contributor:
    fullname: Jessell
– volume: 147
  start-page: 653
  year: 2011
  end-page: 665
  ident: bib48
  article-title: Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template
  publication-title: Cell
  contributor:
    fullname: Jessell
– volume: 47
  start-page: 825
  year: 2009
  end-page: 841
  ident: bib14
  article-title: The evolution of gnathostome development: Insight from chondrichthyan embryology
  publication-title: Genesis
  contributor:
    fullname: Shubin
– volume: 57
  start-page: 147
  year: 2008
  end-page: 161
  ident: bib6
  article-title: Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling
  publication-title: Brain Res. Brain Res. Rev.
  contributor:
    fullname: Cabelguen
– volume: 339
  start-page: 105
  year: 1993
  end-page: 108
  ident: bib21
  article-title: On Bipedalism in Skates and Rays
  publication-title: Philos. Trans. R Soc. B
  contributor:
    fullname: Bone
– volume: 3
  start-page: 191
  year: 2014
  ident: bib53
  article-title: SkateBase, an elasmobranch genome project and collection of molecular resources for chondrichthyan fishes
  publication-title: F1000Res.
  contributor:
    fullname: Polson
– volume: 445
  start-page: 311
  year: 2007
  end-page: 314
  ident: bib7
  article-title: Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning
  publication-title: Nature
  contributor:
    fullname: Shubin
– volume: 134
  start-page: 304
  year: 2008
  end-page: 316
  ident: bib9
  article-title: Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1
  publication-title: Cell
  contributor:
    fullname: Jessell
– volume: 85
  start-page: 131
  year: 2015
  end-page: 144
  ident: bib15
  article-title: Distinct limb and trunk premotor circuits establish laterality in the spinal cord
  publication-title: Neuron
  contributor:
    fullname: Arber
– volume: 134
  start-page: 304
  year: 2008
  ident: 10.1016/j.cell.2018.01.013_bib9
  article-title: Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1
  publication-title: Cell
  doi: 10.1016/j.cell.2008.06.019
  contributor:
    fullname: Dasen
– volume: 8
  start-page: 1494
  year: 2013
  ident: 10.1016/j.cell.2018.01.013_bib18
  article-title: De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2013.084
  contributor:
    fullname: Haas
– volume: 162
  start-page: 338
  year: 2015
  ident: 10.1016/j.cell.2018.01.013_bib34
  article-title: Primacy of Flexor Locomotor Pattern Revealed by Ancestral Reversion of Motor Neuron Identity
  publication-title: Cell
  doi: 10.1016/j.cell.2015.06.036
  contributor:
    fullname: Machado
– volume: 74
  start-page: 975
  year: 2012
  ident: 10.1016/j.cell.2018.01.013_bib2
  article-title: Motor circuits in action: specification, connectivity, and function
  publication-title: Neuron
  doi: 10.1016/j.neuron.2012.05.011
  contributor:
    fullname: Arber
– volume: 9
  start-page: 218
  year: 2009
  ident: 10.1016/j.cell.2018.01.013_bib36
  article-title: Comparative genomics of chondrichthyan Hoxa clusters
  publication-title: BMC Evol. Biol.
  doi: 10.1186/1471-2148-9-218
  contributor:
    fullname: Mulley
– volume: 204
  start-page: 379
  year: 2001
  ident: 10.1016/j.cell.2018.01.013_bib44
  article-title: Pectoral fin locomotion in batoid fishes: undulation versus oscillation
  publication-title: J. Exp. Biol.
  doi: 10.1242/jeb.204.2.379
  contributor:
    fullname: Rosenberger
– volume: 271
  start-page: 1219
  year: 2010
  ident: 10.1016/j.cell.2018.01.013_bib33
  article-title: Comparative punting kinematics and pelvic fin musculature of benthic batoids
  publication-title: J. Morphol.
  doi: 10.1002/jmor.10865
  contributor:
    fullname: Macesic
– volume: 52
  start-page: 751
  year: 2006
  ident: 10.1016/j.cell.2018.01.013_bib16
  article-title: Biological pattern generation: the cellular and computational logic of networks in motion
  publication-title: Neuron
  doi: 10.1016/j.neuron.2006.11.008
  contributor:
    fullname: Grillner
– volume: 68
  start-page: 309
  year: 2008
  ident: 10.1016/j.cell.2018.01.013_bib10
  article-title: Hox genes and the regulation of movement in Drosophila
  publication-title: Dev. Neurobiol.
  doi: 10.1002/dneu.20589
  contributor:
    fullname: Dixit
– volume: 59
  start-page: 226
  year: 2008
  ident: 10.1016/j.cell.2018.01.013_bib45
  article-title: Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons
  publication-title: Neuron
  doi: 10.1016/j.neuron.2008.06.025
  contributor:
    fullname: Rousso
– volume: 85
  start-page: 131
  year: 2015
  ident: 10.1016/j.cell.2018.01.013_bib15
  article-title: Distinct limb and trunk premotor circuits establish laterality in the spinal cord
  publication-title: Neuron
  doi: 10.1016/j.neuron.2014.11.024
  contributor:
    fullname: Goetz
– volume: 343
  start-page: 197
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib4
  article-title: Modular organization of axial microcircuits in zebrafish
  publication-title: Science
  doi: 10.1126/science.1245629
  contributor:
    fullname: Bagnall
– volume: 1
  start-page: 49
  year: 2010
  ident: 10.1016/j.cell.2018.01.013_bib32
  article-title: Ancestry of motor innervation to pectoral fin and forelimb
  publication-title: Nat. Commun.
  doi: 10.1038/ncomms1045
  contributor:
    fullname: Ma
– volume: 87
  start-page: 1008
  year: 2015
  ident: 10.1016/j.cell.2018.01.013_bib20
  article-title: Spinal Locomotor Circuits Develop Using Hierarchical Rules Based on Motorneuron Position and Identity
  publication-title: Neuron
  doi: 10.1016/j.neuron.2015.08.005
  contributor:
    fullname: Hinckley
– volume: 2003
  start-page: 553
  year: 2003
  ident: 10.1016/j.cell.2018.01.013_bib28
  article-title: Punting: An unusual mode of locomotion in the little skate, Leucoraja erinacea (Chondrichthyes: Rajidae)
  publication-title: Copeia
  doi: 10.1643/CG-02-153R1
  contributor:
    fullname: Koester
– volume: 32
  start-page: 408
  year: 2015
  ident: 10.1016/j.cell.2018.01.013_bib22
  article-title: Evolution of patterning systems and circuit elements for locomotion
  publication-title: Dev. Cell
  doi: 10.1016/j.devcel.2015.01.008
  contributor:
    fullname: Jung
– volume: 339
  start-page: 105
  year: 1993
  ident: 10.1016/j.cell.2018.01.013_bib21
  article-title: On Bipedalism in Skates and Rays
  publication-title: Philos. Trans. R Soc. B
  doi: 10.1098/rstb.1993.0007
  contributor:
    fullname: Holst
– volume: 513
  start-page: 54
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib47
  article-title: Developmental plasticity and the origin of tetrapods
  publication-title: Nature
  doi: 10.1038/nature13708
  contributor:
    fullname: Standen
– volume: 26
  start-page: 139
  year: 2010
  ident: 10.1016/j.cell.2018.01.013_bib43
  article-title: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btp616
  contributor:
    fullname: Robinson
– volume: 121
  start-page: 4117
  year: 1995
  ident: 10.1016/j.cell.2018.01.013_bib1
  article-title: Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish
  publication-title: Development
  doi: 10.1242/dev.121.12.4117
  contributor:
    fullname: Appel
– volume: 82
  start-page: 138
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib54
  article-title: V1 and v2b interneurons secure the alternating flexor-extensor motor activity mice require for limbed locomotion
  publication-title: Neuron
  doi: 10.1016/j.neuron.2014.02.013
  contributor:
    fullname: Zhang
– volume: 445
  start-page: 311
  year: 2007
  ident: 10.1016/j.cell.2018.01.013_bib7
  article-title: Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning
  publication-title: Nature
  doi: 10.1038/nature05436
  contributor:
    fullname: Dahn
– volume: 147
  start-page: 653
  year: 2011
  ident: 10.1016/j.cell.2018.01.013_bib48
  article-title: Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template
  publication-title: Cell
  doi: 10.1016/j.cell.2011.10.012
  contributor:
    fullname: Sürmeli
– volume: 10
  start-page: e1004245
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib40
  article-title: A combination of activation and repression by a colinear Hox code controls forelimb-restricted expression of Tbx5 and reveals Hox protein specificity
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1004245
  contributor:
    fullname: Nishimoto
– volume: 14
  start-page: 412
  year: 2012
  ident: 10.1016/j.cell.2018.01.013_bib50
  article-title: Acquisition of the paired fins: a view from the sequential evolution of the lateral plate mesoderm
  publication-title: Evol. Dev.
  doi: 10.1111/j.1525-142X.2012.00561.x
  contributor:
    fullname: Tanaka
– volume: 19
  start-page: 572
  year: 2009
  ident: 10.1016/j.cell.2018.01.013_bib17
  article-title: Measured motion: searching for simplicity in spinal locomotor networks
  publication-title: Curr. Opin. Neurobiol.
  doi: 10.1016/j.conb.2009.10.011
  contributor:
    fullname: Grillner
– volume: 355
  start-page: 164
  year: 2011
  ident: 10.1016/j.cell.2018.01.013_bib37
  article-title: Evolution of motor innervation to vertebrate fins and limbs
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2011.04.009
  contributor:
    fullname: Murakami
– volume: 12
  start-page: e1001773
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib52
  article-title: Conservation and divergence of regulatory strategies at Hox Loci and the origin of tetrapod digits
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.1001773
  contributor:
    fullname: Woltering
– volume: 537
  start-page: 225
  year: 2016
  ident: 10.1016/j.cell.2018.01.013_bib39
  article-title: Digits and fin rays share common developmental histories
  publication-title: Nature
  doi: 10.1038/nature19322
  contributor:
    fullname: Nakamura
– volume: 291
  start-page: 1079
  year: 2008
  ident: 10.1016/j.cell.2018.01.013_bib35
  article-title: Variability and conservation in late chondrichthyan development: ontogeny of the winter skate (Leucoraja ocellata)
  publication-title: Anat. Rec. (Hoboken)
  doi: 10.1002/ar.20719
  contributor:
    fullname: Maxwell
– volume: 334
  start-page: 1517
  year: 2011
  ident: 10.1016/j.cell.2018.01.013_bib26
  article-title: A natural deletion of the HoxC cluster in elasmobranch fishes
  publication-title: Science
  doi: 10.1126/science.1210912
  contributor:
    fullname: King
– volume: 67
  start-page: 781
  year: 2010
  ident: 10.1016/j.cell.2018.01.013_bib23
  article-title: Global control of motor neuron topography mediated by the repressive actions of a single hox gene
  publication-title: Neuron
  doi: 10.1016/j.neuron.2010.08.008
  contributor:
    fullname: Jung
– volume: 32
  start-page: 997
  year: 2001
  ident: 10.1016/j.cell.2018.01.013_bib30
  article-title: Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids
  publication-title: Neuron
  doi: 10.1016/S0896-6273(01)00544-X
  contributor:
    fullname: Liu
– volume: 95
  start-page: 67
  year: 1998
  ident: 10.1016/j.cell.2018.01.013_bib49
  article-title: Specification of motor neuron identity by the MNR2 homeodomain protein
  publication-title: Cell
  doi: 10.1016/S0092-8674(00)81783-3
  contributor:
    fullname: Tanabe
– volume: 29
  start-page: 171
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib24
  article-title: Evolving Hox activity profiles govern diversity in locomotor systems
  publication-title: Dev. Cell
  doi: 10.1016/j.devcel.2014.03.008
  contributor:
    fullname: Jung
– volume: 23
  start-page: 83
  year: 2012
  ident: 10.1016/j.cell.2018.01.013_bib25
  article-title: Eph and ephrin signaling: lessons learned from spinal motor neurons
  publication-title: Semin. Cell Dev. Biol.
  doi: 10.1016/j.semcdb.2011.10.016
  contributor:
    fullname: Kao
– volume: 108
  start-page: 21146
  year: 2011
  ident: 10.1016/j.cell.2018.01.013_bib27
  article-title: Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1118669109
  contributor:
    fullname: King
– volume: 30
  start-page: 2114
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib5
  article-title: Trimmomatic: a flexible trimmer for Illumina sequence data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btu170
  contributor:
    fullname: Bolger
– volume: 529
  start-page: 399
  year: 2016
  ident: 10.1016/j.cell.2018.01.013_bib46
  article-title: Motor neurons control locomotor circuit function retrogradely via gap junctions
  publication-title: Nature
  doi: 10.1038/nature16497
  contributor:
    fullname: Song
– volume: 112
  start-page: 15940
  year: 2015
  ident: 10.1016/j.cell.2018.01.013_bib38
  article-title: Molecular mechanisms underlying the exceptional adaptations of batoid fins
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1521818112
  contributor:
    fullname: Nakamura
– volume: 40
  start-page: 82
  year: 1992
  ident: 10.1016/j.cell.2018.01.013_bib11
  article-title: The spinal motor system in early vertebrates and some of its evolutionary changes
  publication-title: Brain Behav. Evol.
  doi: 10.1159/000113905
  contributor:
    fullname: Fetcho
– volume: 123
  start-page: 477
  year: 2005
  ident: 10.1016/j.cell.2018.01.013_bib8
  article-title: A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity
  publication-title: Cell
  doi: 10.1016/j.cell.2005.09.009
  contributor:
    fullname: Dasen
– volume: 2
  start-page: 2924
  year: 2007
  ident: 10.1016/j.cell.2018.01.013_bib19
  article-title: A manual method for the purification of fluorescently labeled neurons from the mammalian brain
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2007.416
  contributor:
    fullname: Hempel
– volume: 57
  start-page: 147
  year: 2008
  ident: 10.1016/j.cell.2018.01.013_bib6
  article-title: Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling
  publication-title: Brain Res. Brain Res. Rev.
  doi: 10.1016/j.brainresrev.2007.07.006
  contributor:
    fullname: Chevallier
– volume: 47
  start-page: 825
  year: 2009
  ident: 10.1016/j.cell.2018.01.013_bib14
  article-title: The evolution of gnathostome development: Insight from chondrichthyan embryology
  publication-title: Genesis
  doi: 10.1002/dvg.20597
  contributor:
    fullname: Gillis
– volume: 132
  start-page: 4471
  year: 2005
  ident: 10.1016/j.cell.2018.01.013_bib13
  article-title: Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations
  publication-title: Development
  doi: 10.1242/dev.02044
  contributor:
    fullname: Flanagan-Steet
– volume: 80
  start-page: 12
  year: 2013
  ident: 10.1016/j.cell.2018.01.013_bib42
  article-title: Hox genes: choreographers in neural development, architects of circuit organization
  publication-title: Neuron
  doi: 10.1016/j.neuron.2013.09.020
  contributor:
    fullname: Philippidou
– volume: 9
  start-page: e1003184
  year: 2013
  ident: 10.1016/j.cell.2018.01.013_bib29
  article-title: Genetic and functional modularity of Hox activities in the specification of limb-innervating motor neurons
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1003184
  contributor:
    fullname: Lacombe
– volume: 77
  start-page: 35
  year: 2002
  ident: 10.1016/j.cell.2018.01.013_bib31
  article-title: Walking in skates (Chondrichthyes, Rajidae): anatomy, behaviour and analogies to tetrapod locomotion
  publication-title: Biol. J. Linn. Soc. Lond.
  doi: 10.1046/j.1095-8312.2002.00085.x
  contributor:
    fullname: Lucifora
– volume: 3
  start-page: 191
  year: 2014
  ident: 10.1016/j.cell.2018.01.013_bib53
  article-title: SkateBase, an elasmobranch genome project and collection of molecular resources for chondrichthyan fishes
  publication-title: F1000Res.
  doi: 10.12688/f1000research.4996.1
  contributor:
    fullname: Wyffels
– volume: 21
  start-page: 867
  year: 2017
  ident: 10.1016/j.cell.2018.01.013_bib3
  article-title: Columnar-Intrinsic Cues Shape Premotor Input Specificity in Locomotor Circuits
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2017.10.004
  contributor:
    fullname: Baek
– volume: 14
  start-page: 417
  year: 2017
  ident: 10.1016/j.cell.2018.01.013_bib41
  article-title: Salmon provides fast and bias-aware quantification of transcript expression
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.4197
  contributor:
    fullname: Patro
– volume: 6
  start-page: 23711
  year: 2016
  ident: 10.1016/j.cell.2018.01.013_bib12
  article-title: Tetrapod-like pelvic girdle in a walking cavefish
  publication-title: Sci. Rep.
  doi: 10.1038/srep23711
  contributor:
    fullname: Flammang
– volume: 79
  start-page: 957
  year: 1994
  ident: 10.1016/j.cell.2018.01.013_bib51
  article-title: Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes
  publication-title: Cell
  doi: 10.1016/0092-8674(94)90027-2
  contributor:
    fullname: Tsuchida
SSID ssj0008555
Score 2.552268
Snippet Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb...
Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits essential for limb control...
SourceID pubmedcentral
proquest
crossref
pubmed
elsevier
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 667
SubjectTerms Animal Fins - physiology
Animals
Avian Proteins - genetics
Avian Proteins - metabolism
Chick Embryo
Chickens - physiology
development
evolution
Evolution, Molecular
Fish Proteins - genetics
Fish Proteins - metabolism
Homeodomain Proteins - genetics
Homeodomain Proteins - metabolism
Hox gene
locomotion
motor neuron
Muscle, Skeletal - physiology
Nerve Net - physiology
neural circuit
Skates, Fish - physiology
spinal cord
Swimming - physiology
Transcription Factors - genetics
Transcription Factors - metabolism
Walking - physiology
Zebrafish - physiology
Title The Ancient Origins of Neural Substrates for Land Walking
URI https://dx.doi.org/10.1016/j.cell.2018.01.013
https://www.ncbi.nlm.nih.gov/pubmed/29425489
https://search.proquest.com/docview/2001067160
https://pubmed.ncbi.nlm.nih.gov/PMC5808577
Volume 172
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3da9swED_6wWAvo123Nf0IGuytmFiWZMuPaWjI2q55adqwFyPLEk0ZTmmSh_33u_NHaDq6h4FfZFkgfjrdneS73wF8S3zi0W5EgZEuDtBC8CC3Ard7nnNrI6ltTNnIP27i0UReTtV0CwZtLgyFVTa6v9bplbZu3vQaNHtPsxnl-KaRjol9RVSsJtuwS1zmKNq7_fO7q-u1QtZK1YUMUtz8OKDJnanDvOh-nCK8dMXeycVb9ulv__N1GOULuzTcgw-NQ8n69Zz3YcuVH-FdXWLy9wGkKAesX1Zpj2xcVcFasLlnRMqBw0hvVPy0C4beK7s2ZcHuzS-6P_8Ek-HF7WAUNOUSAktVCYLCq0JFMjZaRXmecI_QCPpP5m3ouCickwmVbjPSFqENc5VLY7l0xheaIqvEZ9gp56U7BIbnHKd05OPYGJkIkyoReV5wOq159IE6cNaClD3VrBhZGy72mBGkGUGahRwf0QHV4phtrG2Gavuf4762oGco9NRtSjdfLah2JlHf8TjswJd6EdbziFJUQ1KnHUg2lmf9ARFqb_aUs4eKWFtp4vtPjv5zvsfwnlpVTLc-gZ3l88qdosuyzLuNSHZh-_v0HFs3g-n45x8vpusG
link.rule.ids 230,314,780,784,885,3506,27569,27924,27925,45663,45874
linkProvider Elsevier
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LT9wwEB5RECqXipZHt9DWlXpDEXH8iHNcEGhbFnqBws1yHFssqrKIhQP_npk8VmwRPVTKKY4l65vxzNiZ-Qbgex7ziH4jS5wMOkEPwZPSC9zuZcm9z6TxmqqRT8_06EL-vFJXS3DY18JQWmVn-1ub3ljr7s1-h-b-7WRCNb5FZjSxr4iG1eQNrGA0oFHZV4YHv0_Gc4NslGobGRS4-XFCVzvTpnnR_ThleJmGvZOL1_zTy_jz7zTKZ37peB3edQElG7Zrfg9Lof4Aq22LyccNKFAP2LBuyh7Zr6YL1oxNIyNSDpxGdqPhp50xjF7Z2NUVu3R_6P58Ey6Oj84PR0nXLiHx1JUgqaKqVCa1Myory5xHhEbQf7Lo08BFFYLMqXWbk75KfVqqUjrPZXCxMpRZJbZguZ7W4SMwPOcEZbKotXMyF65QIou84nRaixgDDWCvB8netqwYtk8Xu7EEqSVIbcrxEQNQPY52QbYWzfY_533rQbeo9DTs6jB9mFHvTKK-4zodwHYrhPk6sgLNkDTFAPIF8cw_IELtxZF6ct0QaytDfP_5p_9c71d4Ozo_Hdvxj7OTHVijkSa_2-zC8v3dQ_iM4ct9-aVTzydgv-sy
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=The+Ancient+Origins+of+Neural+Substrates+for+Land+Walking&rft.jtitle=Cell&rft.au=Jung%2C+Heekyung&rft.au=Baek%2C+Myungin&rft.au=D%E2%80%99Elia%2C+Kristen+P.&rft.au=Boisvert%2C+Catherine&rft.date=2018-02-08&rft.issn=0092-8674&rft.volume=172&rft.issue=4&rft.spage=667&rft.epage=682.e15&rft_id=info:doi/10.1016%2Fj.cell.2018.01.013&rft.externalDBID=n%2Fa&rft.externalDocID=10_1016_j_cell_2018_01_013
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0092-8674&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0092-8674&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0092-8674&client=summon