Introduction: The changes in knee axial rotation play an important role in traumatic and non-traumatic knee disorders. It is known that support afferentation can affect the axial rotator muscles. The condition of innervation of the semitendinosus (ST) and biceps femoris posterior (BFp) has changed in non-terrestrial and terrestrial vertebrates in evolution; thus, we hypothesized this situation might be replayed by hindlimb unloading (HU). Methods: In the present study, the EMG activity of two hamstring muscles, m. ST and m. BFp, which are antagonists in axial rotation of the tibia, was examined before and after 7 days of HU. Results: During locomotion and swimming, the ST flexor burst activity increased in the stance-to-swing transition and in the retraction-protraction transition, respectively, while that of BFp remained unchanged. Both ST and BFp non-burst extensor activity increased during stepping and decreased during swimming. Conclusions: Our results show that (1) the flexor burst activity of ST and BFp depends differently on the load-dependent sensory input in the step cycle; (2) shift of the activity gradient towards ST in the stance-to-swing transition could produce excessive internal tibia torque, which can be used as an experimental model of non-traumatic musculoskeletal disorders; and (3) the mechanisms of activity of ST and BFp may be based on reciprocal activity of homologous muscles in primary tetrapodomorph and depend on the increased role of supraspinal control.

1.
Haines
RW
.
The tetrapod knee joint
.
J Anat
.
1942
;
76
(
Pt 3
):
270
301
. doi: .
2.
Senter
C
,
Hame
SL
.
Biomechanical analysis of tibial torque and knee flexion angle: implications for understanding knee injury
.
Sports Med
.
2006
;
36
(
8
):
635
41
. .
3.
Balachandar
V
,
Marciniak
JL
,
Wall
O
,
Balachandar
C
.
Effects of the menstrual cycle on lower-limb biomechanics, neuromuscular control, and anterior cruciate ligament injury risk: a systematic review
.
Muscles Ligaments Tendons J
.
2017
;
7
(
1
):
136
46
. doi: .
4.
Eckhoff
DG
,
Brown
AW
,
Kilcoyne
RF
,
Stamm
ER
.
Knee version associated with anterior knee pain
.
Clin Orthop Relat Res
.
1997
;
339
:
152
5
. doi: .
5.
Bytyqi
D
,
Shabani
B
,
Lustig
S
,
Cheze
L
,
Karahoda Gjurgjeala
N
,
Neyret
P
.
Gait knee kinematic alterations in medial osteoarthritis: three dimensional assessment
.
Int Orthop
.
2014
;
38
(
6
):
1191
8
. doi: .
6.
Toor
AS
,
Limpisvasti
O
,
Ihn
HE
,
McGarry
MH
,
Banffy
M
,
Lee
TQ
.
The significant effect of the medial hamstrings on dynamic knee stability
.
Knee Surg Sports Traumatol Arthrosc
.
2019
;
27
(
8
):
2608
16
. doi: .
7.
Hsu
D
,
Anand
P
,
Mabrouk
A
,
Chang
KV
.
Biceps tendon rupture of the lower limb
.
StatPearls [internet]
.
Treasure Island (FL)
:
StatPearls Publishing
;
2023
.
8.
English
AW
,
Weeks
OI
.
An anatomical and functional analysis of cat biceps femoris and semitendinosus muscles
.
J Morphol
.
1987
;
191
(
2
):
161
75
. doi: .
9.
Diogo
R
,
Bello-Hellegouarch
G
,
Kohlsdorf
T
,
Esteve-Altava
B
,
Molnar
JL
.
Comparative myology and evolution of marsupials and other vertebrates, with notes on complexity, bauplan, and “Scala Naturae”
.
Anat Rec
.
2016
;
299
(
9
):
1224
55
. doi: .
10.
Molnar
JL
,
Diogo
R
,
Hutchinson
JR
,
Pierce
SE
.
Evolution of hindlimb muscle anatomy across the tetrapod water-to-land transition, including comparisons with forelimb anatomy
.
Anat Rec
.
2020
;
303
(
2
):
218
34
. doi: .
11.
Richards
CT
,
Porro
LB
,
Collings
AJ
.
Kinematic control of extreme jump angles in the red-legged running frog, Kassina maculata
.
J Exp Biol
.
2017
;
220
(
Pt 10
):
1894
904
. .
12.
Kargo
WJ
,
Nelson
F
,
Rome
LC
.
Jumping in frogs: assessing the design of the skeletal system by anatomically realistic modeling and forward dynamic simulation
.
J Exp Biol
.
2002
;
205
(
Pt 12
):
1683
702
. doi: .
13.
Brown
NP
,
Bertocci
GE
,
Cheffer
KA
,
Howland
DR
.
A three dimensional multiplane kinematic model for bilateral hind limb gait analysis in cats
.
PLoS One
.
2018
;
13
(
8
):
e0197837
. .
14.
Fu
YC
,
Torres
BT
,
Budsberg
SC
.
Evaluation of a three-dimensional kinematic model for canine gait analysis
.
Am J Vet Res
.
2010
;
71
(
10
):
1118
22
. doi: .
15.
Lafortune
MA
,
Cavanagh
PR
,
Sommer
HJ
3rd
,
Kalenak
A
.
Three-dimensional kinematics of the human knee during walking
.
J Biomech
.
1992
;
25
(
4
):
347
57
. doi: .
16.
Gray
HA
,
Guan
S
,
Thomeer
LT
,
Schache
AG
,
de Steiger
R
,
Pandy
MG
.
Three-dimensional motion of the knee-joint complex during normal walking revealed by mobile biplane x-ray imaging
.
J Orthop Res
.
2019
;
37
(
3
):
615
30
. doi: .
17.
Mayerl
CJ
,
Capano
JG
,
Moreno
AA
,
Wyneken
J
,
Blob
RW
,
Brainerd
EL
.
Pectoral and pelvic girdle rotations during walking and swimming in a semi-aquatic turtle: testing functional role and constraint
.
J Exp Biol
.
2019
;
222
(
Pt 24
):
jeb212688
. doi: .
18.
Hansen
C
,
Einarson
E
,
Thomson
A
,
Whiteley
R
.
Peak medial (but not lateral) hamstring activity is significantly lower during stance phase of running. An EMG investigation using a reduced gravity treadmill
.
Gait Posture
.
2017
;
57
:
7
10
. doi: .
19.
Ariano
MA
,
Armstrong
RB
,
Edgerton
VR
.
Hindlimb muscle fiber populations of five mammals
.
J Histochem Cytochem
.
1973
;
21
(
1
):
51
5
. doi: .
20.
Alford
EK
,
Roy
RR
,
Hodgson
JA
,
Edgerton
VR
.
Electromyography of rat soleus, medial gastrocnemius, and tibialis anterior during hind limb suspension
.
Exp Neurol
.
1987
;
96
(
3
):
635
49
. doi: .
21.
Winiarski
AM
,
Roy
RR
,
Alford
EK
,
Chiang
PC
,
Edgerton
VR
.
Mechanical properties of rat skeletal muscle after hind limb suspension
.
Exp Neurol
.
1987
;
96
(
3
):
650
60
. doi: .
22.
Canu
MH
,
Falempin
M
.
Effect of hindlimb unloading on locomotor strategy during treadmill locomotion in the rat
.
Eur J Appl Physiol Occup Physiol
.
1996
;
74
(
4
):
297
304
. doi: .
23.
Canu
MH
,
Garnier
C
,
Lepoutre
FX
,
Falempin
M
.
A 3D analysis of hindlimb motion during treadmill locomotion in rats after a 14-day episode of simulated microgravity
.
Behav Brain Res
.
2005
;
157
(
2
):
309
21
. doi: .
24.
Tajino
J
,
Ito
A
,
Nagai
M
,
Zhang
X
,
Yamaguchi
S
,
Iijima
H
, et al
.
Intermittent application of hypergravity by centrifugation attenuates disruption of rat gait induced by 2 weeks of simulated microgravity
.
Behav Brain Res
.
2015
;
287
:
276
84
. doi: .
25.
Musienko
P
,
van den Brand
R
,
Märzendorfer
O
,
Roy
RR
,
Gerasimenko
Y
,
Edgerton
VR
, et al
.
Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries
.
J Neurosci
.
2011
;
31
(
25
):
9264
78
. doi: .
26.
Morey-Holton
ER
,
Globus
RK
.
Hindlimb unloading rodent model: technical aspects
.
J Appl Physiol
.
2002
;
92
(
4
):
1367
77
. doi: .
27.
Roy
RR
,
Hutchison
DL
,
Pierotti
DJ
,
Hodgson
JA
,
Edgerton
VR
.
EMG patterns of rat ankle extensors and flexors during treadmill locomotion and swimming
.
J Appl Physiol
.
1991
;
70
(
6
):
2522
9
. doi: .
28.
Philippson
M
.
L’autonomie et la centralisation dans le système nerveux des animaux
.
Trav Lab Physio Inst Solvay Brux
.
1905
;
7
:
1
208
.
29.
Aarts
E
,
Verhage
M
,
Veenvliet
JV
,
Dolan
CV
,
Van Der Sluis
S
.
A solution to dependency: using multilevel analysis to accommodate nested data
.
Nat Neurosci
.
2014
;
17
(
4
):
491
6
. doi: .
30.
Nicolopoulos-Stournaras
S
,
Iles
JF
.
Hindlimb muscle activity during locomotion in the rat (Rattus norvegicus) (Rodentia:Muridae)
.
J Zool Lond
.
1984
;
203
(
3
):
427
40
. doi: .
31.
Peters
SE
,
Goslow
GE
Jr
.
From salamanders to mammals: continuity in musculoskeletal function during locomotion
.
Brain Behav Evol
.
1983
;
22
(
4
):
191
7
. doi: .
32.
Ashley-Ross
MA
.
Patterns of hind limb motor output during walking in the salamander Dicamptodon tenebrosus, with comparisons to other tetrapods
.
J Comp Physiol
.
1995
;
177
(
3
):
273
85
. doi: .
33.
Cohen
AH
.
The role of heterarchical control in the evolution of central pattern generators
.
Brain Behav Evol
.
1992
;
40
(
2–3
):
112
24
. doi: .
34.
Fujita
N
,
Fujimoto
T
,
Tasaki
H
,
Arakawa
T
,
Matsubara
T
,
Miki
A
.
Influence of muscle length on muscle atrophy in the mouse tibialis anterior and soleus muscles
.
Biomed Res
.
2009
;
30
(
1
):
39
45
. doi: .
35.
Kawano
F
,
Ishihara
A
,
Stevens
JL
,
Wang
XD
,
Ohshima
S
,
Horisaka
M
, et al
.
Tension- and afferent input-associated responses of neuromuscular system of rats to hindlimb unloading and/or tenotomy
.
Am J Physiol Regul Integr Comp Physiol
.
2004
;
287
(
1
):
R76
86
. doi: .
36.
Popov
A
,
Lyakhovetskii
V
,
Bazhenova
E
,
Gorskii
O
,
Kalinina
D
,
Merkulyeva
N
, et al
.
The role of load-dependent sensory input in the control of balance during gait in rats
.
J Exp Biol
.
2021
;
224
(
15
):
jeb242138
. doi: .
37.
Schilling
N
,
Fischbein
T
,
Yang
EP
,
Carrier
DR
.
Function of the extrinsic hindlimb muscles in trotting dogs
.
J Exp Biol
.
2009
;
212
(
Pt 7
):
1036
52
. doi: .
38.
Carlson-Kuhta
P
,
Trank
TV
,
Smith
JL
.
Forms of forward quadrupedal locomotion. II. A comparison of posture, hindlimb kinematics, and motor patterns for upslope and level walking
.
J Neurophysiol
.
1998
;
79
(
4
):
1687
701
. doi: .
39.
Martinez
M
,
Tuznik
M
,
Delivet-Mongrain
H
,
Rossignol
S
.
Emergence of deletions during treadmill locomotion as a function of supraspinal and sensory inputs
.
J Neurosci
.
2013
;
33
(
28
):
11599
605
. doi: .
40.
McCrea
DA
,
Rybak
IA
.
Organization of mammalian locomotor rhythm and pattern generation
.
Brain Res Rev
.
2008
;
57
(
1
):
134
46
. doi: .
41.
Treffort
N
,
Picquet
F
,
Petit
J
,
Falempin
M
.
The structure and response properties of golgi tendon organs in control and hypodynamia-hypokinesia rats
.
Exp Neurol
.
2005
;
195
(
2
):
313
21
. doi: .
42.
Gatesy
SM
.
An electromyographic analysis of hindlimb function in Alligator during terrestrial locomotion
.
J Morphol
.
1997
;
234
:
197
212
. doi: .
43.
Mann
RA
,
Hagy
J
.
Biomechanics of walking, running, and sprinting
.
Am J Sports Med
.
1980
;
8
(
5
):
345
50
. doi: .
44.
Deban
SM
,
Schilling
N
,
Carrier
DR
.
Activity of extrinsic limb muscles in dogs at walk, trot and gallop
.
J Exp Biol
.
2012
;
215
(
Pt 2
):
287
300
. doi: .
45.
Reinschmidt
C
,
van den Bogert
AJ
,
Nigg
BM
,
Lundberg
A
,
Murphy
N
.
Effect of skin movement on the analysis of skeletal knee joint motion during running
.
J Biomech
.
1997
;
30
(
7
):
729
32
. doi: .
46.
Bauman
JM
,
Chang
Y-H
.
High-speed X-ray video demonstrates significant skin movement errors with standard optical kinematics during rat locomotion
.
J Neurosci Methods
.
2010
;
186
(
1
):
18
24
. doi: .
47.
Victor
J
,
Labey
L
,
Wong
P
,
Innocenti
B
,
Bellemans
J
.
The influence of muscle load on tibiofemoral knee kinematics
.
J Orthop Res
.
2010
;
28
(
4
):
419
28
. doi: .
You do not currently have access to this content.