 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 13, 4456-4469, Copyright © 1993 by Society for Neuroscience
Two distinct rhythmic motor patterns are driven by common premotor and motor neurons in a simple vertebrate spinal cord
SR Soffe
Department of Zoology, Bristol University, United Kingdom.
Xenopus embryos show two distinct rhythmic motor patterns: swimming and
struggling. Both can be generated by spinal cord circuitry and evoked by
stimulation of a single skin sensory pathway (Soffe, 1991b). This presents
a valuable opportunity to explore mechanisms for vertebrate motor pattern
switching. Swimming and struggling have been compared using intracellular
recording from spinal neurons in immobilized embryos. Underlying synaptic
drive was similar; motoneurons and premotor interneurons were excited in
phase with ipsilateral motor root discharge and inhibited in phase with
contralateral motor root discharge. Excitation was stronger during
struggling and associated with short bursts of impulses, contrasting with
single spikes per cycle during swimming. Excitation was reduced in both
patterns by local application of 1 mM kynurenic acid, indicating excitatory
amino acid mediation. Inhibition was antagonized by 1 microM strychnine,
indicating glycine mediation. Many motoneurons (76%) and premotor
interneurons (68%) fired during both swimming and struggling, including
examples of all three spinal premotor interneuron classes. Most of the
remaining motoneurons (20%) and premotor interneurons (24%) fired only
during struggling, providing roughly 30% more active neurons than during
swimming. To investigate whether new neuronal classes become active during
struggling, recordings were made from sensory neurons and sensory
interneurons. Rohon-Beard sensory neurons did not fire during either
swimming or struggling. Dorsolateral commissural sensory interneurons
received rhythmic, strychnine-sensitive inhibition during both swimming and
struggling and also did not fire. Neither of these neuronal classes is
therefore recruited to the circuitry for struggling. Although behaviorally
distinct, Xenopus embryo swimming and struggling motor patterns appear to
employ similar synaptic drive. I propose that this reflects the common
nature of much of the premotor circuitry that drives them. Extra neurons
are recruited to this circuitry during struggling, but only from within
classes that also participate in swimming.
This article has been cited by other articles:
|
|
|
|
 
A. Berkowitz
Physiology and Morphology of Shared and Specialized Spinal Interneurons for Locomotion and Scratching
J Neurophysiol,
June 1, 2008;
99(6):
2887 - 2901.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Sasaki, J. Jing, M. R. Due, and K. R. Weiss
An Input-Representing Interneuron Regulates Spike Timing and Thereby Phase Switching in a Motor Network
J. Neurosci.,
February 20, 2008;
28(8):
1916 - 1928.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-C. Li, B. Sautois, A. Roberts, and S. R. Soffe
Reconfiguration of a Vertebrate Motor Network: Specific Neuron Recruitment and Context-Dependent Synaptic Plasticity
J. Neurosci.,
November 7, 2007;
27(45):
12267 - 12276.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Berkowitz
Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex
J. Neurosci.,
April 25, 2007;
27(17):
4634 - 4641.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Liao
The role of the lateral line and vision on body kinematics and hydrodynamic preference of rainbow trout in turbulent flow
J. Exp. Biol.,
October 15, 2006;
209(20):
4077 - 4090.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Kimura, Y. Okamura, and S.-i. Higashijima
alx, a Zebrafish Homolog of Chx10, Marks Ipsilateral Descending Excitatory Interneurons That Participate in the Regulation of Spinal Locomotor Circuits
J. Neurosci.,
May 24, 2006;
26(21):
5684 - 5697.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Berkowitz
Physiology and Morphology Indicate That Individual Spinal Interneurons Contribute to Diverse Limb Movements
J Neurophysiol,
December 1, 2005;
94(6):
4455 - 4470.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. C. K. Cheung, A. d'Avella, M. C. Tresch, and E. Bizzi
Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors
J. Neurosci.,
July 6, 2005;
25(27):
6419 - 6434.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. A. Masino and J. R. Fetcho
Fictive Swimming Motor Patterns in Wild Type and Mutant Larval Zebrafish
J Neurophysiol,
June 1, 2005;
93(6):
3177 - 3188.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-C. Li, S. R. Soffe, and A. Roberts
Dorsal Spinal Interneurons Forming a Primitive, Cutaneous Sensory Pathway
J Neurophysiol,
August 1, 2004;
92(2):
895 - 904.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-C. Li, S.-i. Higashijima, D. M. Parry, A. Roberts, and S. R. Soffe
Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord
J. Neurosci.,
June 23, 2004;
24(25):
5840 - 5848.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. D. Merrywest, D. L. McLean, J. T. Buchanan, and K. T. Sillar
Evolutionary Divergence in Developmental Strategies and Neuromodulatory Control Systems of Two Amphibian Locomotor Networks
Integr. Comp. Biol.,
February 1, 2004;
44(1):
47 - 56.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-C. Li, S. R. Soffe, and A. Roberts
The Spinal Interneurons and Properties of Glutamatergic Synapses in a Primitive Vertebrate Cutaneous Flexion Reflex
J. Neurosci.,
October 8, 2003;
23(27):
9068 - 9077.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-C. Li, S. R. Soffe, and A. Roberts
Spinal Inhibitory Neurons that Modulate Cutaneous Sensory Pathways during Locomotion in a Simple Vertebrate
J. Neurosci.,
December 15, 2002;
22(24):
10924 - 10934.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. Ritter, D. H. Bhatt, and J. R. Fetcho
In Vivo Imaging of Zebrafish Reveals Differences in the Spinal Networks for Escape and Swimming Movements
J. Neurosci.,
November 15, 2001;
21(22):
8956 - 8965.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Berkowitz
Rhythmicity of Spinal Neurons Activated During Each Form of Fictive Scratching in Spinal Turtles
J Neurophysiol,
August 1, 2001;
86(2):
1026 - 1036.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. M. Earhart and P. S. G. Stein
Step, Swim, and Scratch Motor Patterns in the Turtle
J Neurophysiol,
November 1, 2000;
84(5):
2181 - 2190.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Juranek and S. N. Currie
Electrically Evoked Fictive Swimming in the Low-Spinal Immobilized Turtle
J Neurophysiol,
January 1, 2000;
83(1):
146 - 155.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. M. Earhart and P. S. G. Stein
Scratch-Swim Hybrids in the Spinal Turtle: Blending of Rostral Scratch and Forward Swim
J Neurophysiol,
January 1, 2000;
83(1):
156 - 165.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Combes, P. Meyrand, and J. Simmers
Dynamic Restructuring of a Rhythmic Motor Program by a Single Mechanoreceptor Neuron in Lobster
J. Neurosci.,
May 1, 1999;
19(9):
3620 - 3628.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. PERRINS and S. R. SOFFE
Influence of Glycinergic Inhibition on Spinal Neuron Excitability during Amphibian Tadpole Locomotion
Ann. N.Y. Acad. Sci.,
November 16, 1998;
860(1):
472 - 474.
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Juranek and W. Metzner
Segregation of Behavior-Specific Synaptic Inputs to a Vertebrate Neuronal Oscillator
J. Neurosci.,
November 1, 1998;
18(21):
9010 - 9019.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K.-G. Westberg, P. Clavelou, G. Sandstrom, and J. P. Lund
Evidence that Trigeminal Brainstem Interneurons Form Subpopulations to Produce Different Forms of Mastication in the Rabbit
J. Neurosci.,
August 15, 1998;
18(16):
6466 - 6479.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. S. Green and S. R. Soffe
Roles of Ascending Inhibition During Two Rhythmic Motor Patterns in Xenopus Tadpoles
J Neurophysiol,
May 1, 1998;
79(5):
2316 - 2328.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. M. Kuenzi and N. Dale
The Pharmacology and Roles of two K+ Channels in Motor Pattern Generation in the Xenopus Embryo
J. Neurosci.,
February 15, 1998;
18(4):
1602 - 1612.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Nargeot, D. A. Baxter, and J. H. Byrne
Contingent-Dependent Enhancement of Rhythmic Motor Patterns: An In Vitro Analog of Operant Conditioning
J. Neurosci.,
November 1, 1997;
17(21):
8093 - 8105.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. G. Morris and S. L. Hooper
Muscle Response to Changing Neuronal Input in the Lobster (Panulirus interruptus) Stomatogastric System: Spike Number- versus Spike Frequency-Dependent Domains
J. Neurosci.,
August 1, 1997;
17(15):
5956 - 5971.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. M. Blitz and M. P. Nusbaum
Motor Pattern Selection via Inhibition of Parallel Pathways
J. Neurosci.,
July 1, 1997;
17(13):
4965 - 4975.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. A. DiNardo and J. B. Travers
Distribution of Fos-Like Immunoreactivity in the Medullary Reticular Formation of the Rat after Gustatory Elicited Ingestion and Rejection Behaviors
J. Neurosci.,
May 15, 1997;
17(10):
3826 - 3839.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M.-S. Rioult-Pedotti
Intrinsic NMDA-Induced Oscillations in Motoneurons of an Adult Vertebrate Spinal Cord Are Masked by Inhibition
J Neurophysiol,
February 1, 1997;
77(2):
717 - 730.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
