Twisting and bending: the functional role of salamander lateral hypaxial musculature during locomotion.

The function of the lateral hypaxial muscles during locomotion in tetrapods is controversial. Currently, there are two hypotheses of lateral hypaxial muscle function. The first, supported by electromyographic (EMG) data from a lizard (Iguana iguana) and a salamander (Dicamptodon ensatus), suggests that hypaxial muscles function to bend the body during swimming and to resist long-axis torsion during walking. The second, supported by EMG data from lizards during relatively high-speed locomotion, suggests that these muscles function primarily to bend the body during locomotion, not to resist torsional forces. To determine whether the results from D. ensatus hold for another salamander, we recorded lateral hypaxial muscle EMGs synchronized with body and limb kinematics in the tiger salamander Ambystoma tigrinum. In agreement with results from aquatic locomotion in D. ensatus, all four layers of lateral hypaxial musculature were found to show synchronous EMG activity during swimming in A. tigrinum. Our findings for terrestrial locomotion also agree with previous results from D. ensatus and support the torsion resistance hypothesis for terrestrial locomotion. We observed asynchronous EMG bursts of relatively high intensity in the lateral and medial pairs of hypaxial muscles during walking in tiger salamanders (we call these 'alpha-bursts'). We infer from this pattern that the more lateral two layers of oblique hypaxial musculature, Mm. obliquus externus superficialis (OES) and obliquus externus profundus (OEP), are active on the side towards which the trunk is bending, while the more medial two layers, Mm. obliquus internus (OI) and transversus abdominis (TA), are active on the opposite side. This result is consistent with the hypothesis proposed for D. ensatus that the OES and OEP generate torsional moments to counteract ground reaction forces generated by forelimb support, while the OI and TA generate torsional moments to counteract ground reaction forces from hindlimb support. However, unlike the EMG pattern reported for D. ensatus, a second, lower-intensity burst of EMG activity ('beta-burst') was sometimes recorded from the lateral hypaxial muscles in A. tigrinum. As seen in other muscle systems, these beta-bursts of hypaxial muscle coactivation may function to provide fine motor control during locomotion. The presence of asynchronous, relatively high-intensity alpha-bursts indicates that the lateral hypaxial muscles generate torsional moments during terrestrial locomotion, but it is possible that the balance of forces from both alpha- and beta-bursts may allow the lateral hypaxial muscles to contribute to lateral bending of the body as well.

[1]  G. Loeb,et al.  Electromyography for Experimentalists , 1986 .

[2]  P. Thompson Electromyography for Experimentalists , 1987 .

[3]  G. E. Goslow,et al.  The Avian Shoulder: An Experimental Approach , 1989 .

[4]  D. Carrier,et al.  Activity of the hypaxial muscles during walking in the lizard Iguana iguana. , 1990, The Journal of experimental biology.

[5]  J. Smith,et al.  Adaptive control for backward quadrupedal walking. II. Hindlimb muscle synergies. , 1990, Journal of neurophysiology.

[6]  L. M. Frolich,et al.  KINEMATIC AND ELECTROMYOGRAPHIC ANALYSIS OF THE FUNCTIONAL ROLE OF THE BODY AXIS DURING TERRESTRIAL AND AQUATIC LOCOMOTION IN THE SALAMANDER AMBYSTOMA TIGRINUM , 1992 .

[7]  D. Carrier ACTION OF THE HYPAXIAL MUSCLES DURING WALKING AND SWIMMING IN THE SALAMANDER DICAMPTODON ENSATUS , 1993 .

[8]  P. Aerts,et al.  The Timing of Muscle Strain and Activation During Steady Swimming in a Salamander, Ambystoma Mexicanum , 1995 .

[9]  Ritter,et al.  Epaxial muscle function during locomotion in a lizard (Varanus salvator) and the proposal of a key innovation in the vertebrate axial musculoskeletal system , 1995, The Journal of experimental biology.

[10]  Ritter,et al.  Axial muscle function during lizard locomotion , 1996, The Journal of experimental biology.

[11]  D. Carrier Function of the intercostal muscles in trotting dogs: ventilation or locomotion? , 1996, The Journal of experimental biology.

[12]  John H. Long,et al.  The Importance of Body Stiffness in Undulatory Propulsion , 1996 .

[13]  G. Lauder,et al.  Motor patterns and kinematics during backward walking in the pacific giant salamander: evidence for novel motor output. , 1997, Journal of neurophysiology.

[14]  Gillis,et al.  Anguilliform locomotion in an elongate salamander (Siren intermedia): effects of speed on axial undulatory movements , 1997, The Journal of experimental biology.

[15]  J. Cabelguen,et al.  Epaxial and limb muscle activity during swimming and terrestrial stepping in the adult newt, Pleurodeles waltl. , 1997, Journal of neurophysiology.

[16]  J B Nielsen,et al.  Co-contraction of antagonistic muscles in man. , 1998, Danish medical bulletin.

[17]  Hale,et al.  Mechanics of the fast-start: muscle function and the role of intramuscular pressure in the escape behavior of amia calva and polypterus palmas , 1998, The Journal of experimental biology.

[18]  J. H. Long Muscles, Elastic Energy, and the Dynamics of Body Stiffness in Swimming Eels' , 1998 .

[19]  Brainerd Mechanics of lung ventilation in a large aquatic salamander, siren lacertina , 1998, The Journal of experimental biology.

[20]  R. S. Simons,et al.  Morphological variation of hypaxial musculature in salamanders (Lissamphibia: Caudata) , 1999, Journal of morphology.

[21]  A. Biewener,et al.  Dynamics of muscle function during locomotion: accommodating variable conditions. , 1999, The Journal of experimental biology.

[22]  B. R. Moon Testing an inference of function from structure: Snake vertebrae do the twist , 1999, Journal of morphology.

[23]  Confirmation of the Passive Exhalation Hypothesis for a Terrestrial Caecilian, Dermophis mexicanus , 1999 .

[24]  The Evolution of the Functional Role of Trunk Muscles During Locomotion in Adult Amphibians1 , 2000 .

[25]  R. S. Simons,et al.  Morphology and Function of Lateral Hypaxial Musculature in Salamanders1 , 2000 .

[26]  Adam P. Summers,et al.  The Evolution of the Functional Role of Trunk Muscles During Locomotion in Adult Amphibians1 , 2000 .

[27]  R. S. Simons,et al.  Morphology and Function of Lateral Hypaxial Musculature in Salamanders , 2000 .