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The Journal of Neuroscience, February 1, 2006, 26(5):1470-1485; doi:10.1523/JNEUROSCI.3691-05.2006

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Behavioral/Systems/Cognitive
Neuromechanics of Coordination during Swallowing in Aplysia californica

Hui Ye,¹ Douglas W. Morton,² and Hillel J. Chiel^1,2,3

¹Departments of Biomedical Engineering, ²Neuroscience, and ³Biology, Case Western Reserve University, Cleveland, Ohio 44106-7080

Correspondence should be addressed to Dr. Hillel J. Chiel, Department of Biology, DeGrace 304, Case Western Reserve University, 2080 Adelbert Road, Cleveland, OH 44106-7080. Email: hjc{at}case.edu

Bernstein (1967) hypothesized that preparation of the periphery was crucial for correct responses to motor output. To test this hypothesis in a behaving animal, we examined the roles of two identified motor neurons, B7 and B8, which contribute to feeding behavior in the marine mollusk Aplysia californica. Neuron B7 innervates a hinge muscle and has no overt behavioral effect during smaller-amplitude (type A) swallows, because the hinge muscle is too short to exert force. Neuron B8 activates a muscle (I4) that acts solely to grasp material during type A swallows. During larger-amplitude (type B) swallows, the behavioral actions of both motor neurons change, because the larger-amplitude anterior movement of the grasper sets up the periphery to respond differently to motor outputs. The larger anterior movement stretches the hinge muscle, so that activating neuron B7 mediates the initial retraction phase of swallowing. The changed position of the I4 muscle allows neuron B8 not only to induce grasping but also to pull material into the buccal cavity, contributing to retraction. Thus, larger-amplitude swallows are associated with the expression of two new degrees of freedom (use of the hinge to retract and use of the grasper to retract) that are essential for mediating type B swallows. These results provide a direct demonstration of Bernstein's hypothesis that properly positioning the periphery can be crucial for its ability to correctly respond to motor output and also demonstrate that biomechanical context can alter the functions of identified motor neurons.

Key words: Aplysia; motor coordination; pattern generator; mechanical context; biomechanics; feeding

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Received Oct. 11, 2004; revised Dec. 22, 2004; accepted Dec. 22, 2005.

Correspondence should be addressed to Dr. Hillel J. Chiel, Department of Biology, DeGrace 304, Case Western Reserve University, 2080 Adelbert Road, Cleveland, OH 44106-7080. Email: hjc{at}case.edu

This article has been cited by other articles:

				H. J. Chiel, L. H. Ting, O. Ekeberg, and M. J. Z. Hartmann The Brain in Its Body: Motor Control and Sensing in a Biomechanical Context J. Neurosci., October 14, 2009; 29(41): 12807 - 12814. [Abstract] [Full Text] [PDF]

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				D. A. Baxter and J. H. Byrne Feeding behavior of Aplysia: A model system for comparing cellular mechanisms of classical and operant conditioning Learn. Mem., November 1, 2006; 13(6): 669 - 680. [Abstract] [Full Text] [PDF]

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