 |
The Journal of Neuroscience, June 22, 2005, 25(25):6025-6035; doi:10.1523/JNEUROSCI.0696-05.2005
 Previous Article
Behavioral/Systems/Cognitive
Propriospinal Circuitry Underlying Interlimb Coordination in Mammalian Quadrupedal Locomotion
Laurent Juvin,
John Simmers, and
Didier Morin
Laboratoire de Physiologie et Physiopathologie de la Signalisation Cellulaire, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5543, Equipe Neurophysiologie Adaptative des Systèmes Moteurs, 33076 Bordeaux, France
Soon after birth, freely moving quadrupeds can express locomotor activity with coordinated forelimb and hindlimb movements. To investigate the neural mechanisms underlying this coordination, we used an isolated spinal cord preparation from neonatal rats. Under bath-applied 5-HT, N-methyl-D,L-aspartate (NMA), and dopamine (DA), the isolated cord generates fictive locomotion in which homolateral cervicolumbar extensor motor bursts occur in phase opposition, as does bursting in homologous (left-right) extensor motoneurons. This coordination corresponded to a walking gait monitored with EMG recordings in the freely behaving animal. Functional decoupling of the cervical and lumbar generators in vitro by sucrose blockade at the thoracic cord level revealed independent rhythmogenic capabilities with similar cycle frequencies in the two locomotor regions. When the cord was partitioned at different thoracic levels and 5-HT/NMA/DA was applied to the more caudal compartment, the ability of the lumbar generators to drive their cervical counterparts increased with the proportion of chemically exposed thoracic segments. Blockade of synaptic inhibition at the lumbar level caused synchronous bilateral lumbar rhythmicity that, surprisingly, also was able to impose bilaterally synchronous bursting at the unblocked cervical level. Furthermore, after a midsagittal section from spinal segments C1 to T7, and during additional blockade of cervical synaptic inhibition, the cord exposed to 5-HT/NMA/DA continued to produce a coordinated fictive walking pattern similar to that observed in control. Thus, in the newborn rat, a caudorostral propriospinal excitability gradient appears to mediate interlimb coordination, which relies more on asymmetric axial connectivity (both excitatory and inhibitory) between the lumbar and cervical generators than on differences in their inherent rhythmogenic capacities.
Key words: locomotion; neuronal network interactions; newborn rat; spinal cord; forelimb; hindlimb; in vitro
Received Feb 21, 2005;
revised May 9, 2005;
accepted May 10, 2005.
This article has been cited by other articles:
|
|
|
|
 
A. Bonnot, N. Chub, A. Pujala, and M. J. O'Donovan
Excitatory Actions of Ventral Root Stimulation During Network Activity Generated by the Disinhibited Neonatal Mouse Spinal Cord
J Neurophysiol,
June 1, 2009;
101(6):
2995 - 3011.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Gerasimenko, P. Musienko, I. Bogacheva, T. Moshonkina, A. Savochin, I. Lavrov, R. R. Roy, and V. R. Edgerton
Propriospinal Bypass of the Serotonergic System That Can Facilitate Stepping
J. Neurosci.,
April 29, 2009;
29(17):
5681 - 5689.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. C. Cowley, E. Zaporozhets, R. A. Joundi, and B. J. Schmidt
Contribution of Commissural Projections to Bulbospinal Activation of Locomotion in the In Vitro Neonatal Rat Spinal Cord
J Neurophysiol,
March 1, 2009;
101(3):
1171 - 1178.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. S. Marigold and J. E. Misiaszek
Whole-Body Responses: Neural Control and Implications for Rehabilitation and Fall Prevention
Neuroscientist,
February 1, 2009;
15(1):
36 - 46.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. K. Patrick, J. A. Noah, and J. F. Yang
Interlimb Coordination in Human Crawling Reveals Similarities in Development and Neural Control With Quadrupeds
J Neurophysiol,
February 1, 2009;
101(2):
603 - 613.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Crenna, I. Carpinella, L. Lopiano, A. Marzegan, M. Rabuffetti, M. Rizzone, M. Lanotte, and M. Ferrarin
Influence of basal ganglia on upper limb locomotor synergies. Evidence from deep brain stimulation and L-DOPA treatment in Parkinson's disease
Brain,
December 1, 2008;
131(12):
3410 - 3420.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Beyeler, C. Metais, D. Combes, J. Simmers, and D. Le Ray
Metamorphosis-Induced Changes in the Coupling of Spinal Thoraco-Lumbar Motor Outputs During Swimming in Xenopus laevis
J Neurophysiol,
September 1, 2008;
100(3):
1372 - 1383.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. T. Gordon, M. J. Dunbar, K. J. Vanneste, and P. J. Whelan
Interaction Between Developing Spinal Locomotor Networks in the Neonatal Mouse
J Neurophysiol,
July 1, 2008;
100(1):
117 - 128.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. T. Gordon and P. J. Whelan
Brainstem modulation of locomotion in the neonatal mouse spinal cord
J. Physiol.,
May 15, 2008;
586(10):
2487 - 2497.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Giraudin, M.-J. Cabirol-Pol, J. Simmers, and D. Morin
Intercostal and Abdominal Respiratory Motoneurons in the Neonatal Rat Spinal Cord: Spatiotemporal Organization and Responses to Limb Afferent Stimulation
J Neurophysiol,
May 1, 2008;
99(5):
2626 - 2640.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. F. Samara and S. N. Currie
Location of Spinal Cord Pathways That Control Hindlimb Movement Amplitude and Interlimb Coordination During Voluntary Swimming in Turtles
J Neurophysiol,
April 1, 2008;
99(4):
1953 - 1968.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. C. Cowley, E. Zaporozhets, and B. J. Schmidt
Propriospinal neurons are sufficient for bulbospinal transmission of the locomotor command signal in the neonatal rat spinal cord
J. Physiol.,
March 15, 2008;
586(6):
1623 - 1635.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Pijpers, B. H. J. Winkelman, R. Bronsing, and T. J. H. Ruigrok
Selective Impairment of the Cerebellar C1 Module Involved in Rat Hind Limb Control Reduces Step-Dependent Modulation of Cutaneous Reflexes
J. Neurosci.,
February 27, 2008;
28(9):
2179 - 2189.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. F. Samara and S. N. Currie
Crossed Commissural Pathways in the Spinal Hindlimb Enlargement Are Not Necessary for Right Left Hindlimb Alternation During Turtle Swimming
J Neurophysiol,
October 1, 2007;
98(4):
2223 - 2231.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. P. Zehr, M. Klimstra, K. Dragert, Y. Barzi, M. G. Bowden, B. Javan, and C. Phadke
Enhancement of Arm and Leg Locomotor Coupling With Augmented Cutaneous Feedback From the Hand
J Neurophysiol,
September 1, 2007;
98(3):
1810 - 1814.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Juvin, J. Simmers, and D. Morin
Locomotor rhythmogenesis in the isolated rat spinal cord: a phase-coupled set of symmetrical flexion extension oscillators
J. Physiol.,
August 15, 2007;
583(1):
115 - 128.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. A. Quinlan and O. Kiehn
Segmental, Synaptic Actions of Commissural Interneurons in the Mouse Spinal Cord
J. Neurosci.,
June 13, 2007;
27(24):
6521 - 6530.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Zhong, M. A. Masino, and R. M. Harris-Warrick
Persistent Sodium Currents Participate in Fictive Locomotion Generation in Neonatal Mouse Spinal Cord
J. Neurosci.,
April 25, 2007;
27(17):
4507 - 4518.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Falgairolle and J.-R. Cazalets
Metachronal coupling between spinal neuronal networks during locomotor activity in newborn rat
J. Physiol.,
April 1, 2007;
580(1):
87 - 102.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Yakovenko, J. Kowalczewski, and A. Prochazka
Intraspinal Stimulation Caudal to Spinal Cord Transections in Rats. Testing the Propriospinal Hypothesis
J Neurophysiol,
March 1, 2007;
97(3):
2570 - 2574.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. E. Balter and E. P. Zehr
Neural Coupling Between the Arms and Legs During Rhythmic Locomotor-Like Cycling Movement
J Neurophysiol,
February 1, 2007;
97(2):
1809 - 1818.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Zaporozhets, K. C. Cowley, and B. J. Schmidt
Propriospinal neurons contribute to bulbospinal transmission of the locomotor command signal in the neonatal rat spinal cord
J. Physiol.,
April 15, 2006;
572(2):
443 - 458.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Zhong, M. Diaz-Rios, and R. M. Harris-Warrick
Serotonin Modulates the Properties of Ascending Commissural Interneurons in the Neonatal Mouse Spinal Cord
J Neurophysiol,
March 1, 2006;
95(3):
1545 - 1555.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
