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The Journal of Neuroscience, January 23, 2008, 28(4):868-879; doi:10.1523/JNEUROSCI.4250-07.2008

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Behavioral/Systems/Cognitive
Neuronal Substrates for State-Dependent Changes in Coordination between Motoneuron Pools during Fictive Locomotion in the Lamprey Spinal Cord

Tim Mentel,¹ Lorenzo Cangiano,² Sten Grillner,² and Ansgar Büschges¹

¹Department of Animal Physiology, Zoological Institute, University of Cologne, 50923 Cologne, North-Rhine-Westfalia, Germany, and ²Department of Neuroscience, Karolinska Institutet, SE-17177 Stockholm, Sweden

Correspondence should be addressed to Dr. Ansgar Büschges, Department of Animal Physiology, Zoological Institute, University of Cologne, 50923 Cologne, Germany. Email: ansgar.bueschges{at}uni-koeln.de

Locomotion relies on a precisely timed activation of sets of motoneurons. A fundamental question is how this is achieved. In the lamprey, fin and myotomal motoneurons located on the same side of the spinal cord display alternating activity during straight swimming. The neural mechanism underlying this alternation is studied here during fictive locomotion induced by superfusion with NMDA, or locomotor bursting induced by electrical stimulation. If the spinal cord is split longitudinally, each hemicord still displays rhythmic locomotor related burst activity, but now fin and myotomal motoneurons become active in-phase. The out-of-phase activation of fin motoneurons persists only when at least three segments are left intact in the rostral part of the spinal cord. Proper coordination of fin motoneurons thus requires input from contralateral rostral segments. We show that commissural excitatory interneurons with long descending axons, previously reported to be active in phase with their ipsilateral myotomal motoneurons, provide monosynaptic excitation to contralateral fin motoneurons. Together, these results strongly indicate that, although myotomal motoneurons receive their phasic excitation from ipsilateral excitatory interneurons, fin motoneurons are mainly driven from the contralateral segmental network during bilateral locomotor activity. However, during unilateral bursting, fin and myotomal motoneurons instead receive a common input, which is apparently masked during normal fictive swimming. The spinal organization thus also provides circuitry for different patterns of coordination, i.e., alternation or coactivation of the two pools of motoneurons, which may subserve different forms of locomotor behavior.

Key words: central pattern generation; fin motoneuron; intersegmental coordination; intrasegmental coordination; motor pattern generation; spinal cord

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Received June 18, 2007; revised Nov. 28, 2007; accepted Nov. 28, 2007.

Correspondence should be addressed to Dr. Ansgar Büschges, Department of Animal Physiology, Zoological Institute, University of Cologne, 50923 Cologne, Germany. Email: ansgar.bueschges{at}uni-koeln.de

This article has been cited by other articles:

				E. Jankowska, B. A. Bannatyne, K. Stecina, I. Hammar, A. Cabaj, and D. J. Maxwell Commissural interneurons with input from group I and II muscle afferents in feline lumbar segments: neurotransmitters, projections and target cells J. Physiol., January 15, 2009; 587(2): 401 - 418. [Abstract] [Full Text] [PDF]

				Z. Biro, R. H. Hill, and S. Grillner The Activity of Spinal Commissural Interneurons During Fictive Locomotion in the Lamprey J Neurophysiol, August 1, 2008; 100(2): 716 - 722. [Abstract] [Full Text] [PDF]

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Comments on network organisation

David Parker

J. Neurosci. Online, 30 Jan 2008 [Full text]

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