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Neuronal and biomechanical mechanisms underlying the control and plasticity of aimed limb movements

Principal Supervisor: Dr Tom Matheson, Department of Neuroscience, Psychology and Behaviour

Co-supervisor: Dr Swidbert Ott, Department of Neuroscience, Psychology and Behaviour and Dr Jingzhe Pan, Engineering

PhD project title: Neuronal and biomechanical mechanisms underlying the control and plasticity of aimed limb movements

University of Registration: University of Leicester

Project outline:

Most animal movements are driven by muscle contractions controlled by the nervous system, but there is now considerable evidence that passive forces, originating in muscles, tendons or other tissues, interact with active forces to generate limb movements in both vertebrates and invertebrates (Page et al. 2008). We developed a neuromechanical model (simulation) of the locust hind leg that predicted an important role for passive forces in generating aimed limb movements (Zakotnik et al. 2006), and have now shown experimentally that meaningful movements can indeed be generated by passive forces. Very surprisingly, some of these forces arise within joints themselves and not in the muscles or tendons (Ache & Matheson, 2012, 2013). These passive joint forces move the leg in the absence of motor control (and even in the absence of muscles). Across species, where antagonist muscles have different strengths, passive joint forces support the weaker muscle. We therefore suggest that passive joint forces are shaped by evolutionary adaptation and form an important component of effective motor control.

In related work we have shown that locusts 'recalibrate' their aimed limb movements following experimental disruption of joint proprioceptors. This plasticity allows animals to regain accurate movements in the face of sensory loss. Young adult locusts can similarly adjust their movements following the loss of part of a limb (Gunderson et al. 2011). Older adults do not readjust their movements, indicating that the ability to express plastic changes in motor control varies with age. This is extremely interesting in light of our demonstration that during swarm formation (when locusts undergo remarkable plastic changes in morphology and behaviour collectively known as ‘phase change’) there are marked alterations of walking gait and posture (Blackburn et al. 2010).

This PhD project will merge these strands of research to seek the mechanisms governing plasticity of motor control using our powerful locust phase change model system. The student will measure active and passive limb forces in a range of species to test further our hypothesis that passive joint forces are matched to active forces acting at the same joint. Limb morphology and function will be investigated using micro CT-scanning, coupled with finite element analysis. Our predictive model will be iteratively modified to incorporate passive joint forces, and used to examine experimentally intractable questions. The model will be extended to simulate limbs that have different geometries, behavioural functions and patterns of motor control. Is our current understanding of the interplay of forces sufficiently robust to enable the model to predict the movements generated by different limbs subject to specific patterns of natural motor output? The project will investigate changes in passive forces in animals that learn new movement strategies to deal with limb damage. Is neuronal plasticity matched by plasticity in biomechanical properties? Do passive biomechanical properties change during development? Do our new results generalise across different limb joints? How does inhibitory motor control (Calas-List et al. 2013) bias passive muscle properties? Does the induction of phase change induce motor plasticity in older adult locusts? Are changes in neuromodulator levels during phase change (Rogers et al. 2004; Anstey et al. 2009) important in regulating this motor plasticity?

In this Systems Biology project the student will be trained in both in vivo techniques (behavioural, biomechanical and electrophysiological experiments) and mathematical modelling. The modelling will be supported through a longstanding collaboration with Prof Volker Dürr in the Department of Biological Cybernetics at the University of Bielefeld, and a new collaboration with Jingzhe Pan in the College of Science and Engineering. The project will thus use analysis techniques drawn from distinct behavioural, engineering and neurobiological disciplines to address fundamental questions in limb motor control, viewed from a comparative (evolutionary) functional perspective.

References:

  1. Ache JM and Matheson T (2013) Passive joint forces are tuned to limb use in insects and drive movements without motor activity. Current Biology 23: 1418-1426. doi: 10.1016/j.cub.2013.06.024
  2. Ache JM and Matheson T (2012) Passive resting state and history of antagonist muscle activity shape active extensions in an insect limb. Journal of Neurophysiology 107: 2756-2768. doi: 10.1152/jn.01072.2011
  3. Anstey ML, Rogers SM, Ott SR, Burrows M, Simpson SJ (2009) Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323 (5914): 627-30. doi: 10.1126/science.1165939
  4. Blackburn LM, Ott SR, Matheson T, Burrows M and Rogers SM (2010) Motor neurone responses during a postural reflex in solitarious and gregarious desert locusts. Journal of Insect Physiology 56: 902-910. DOI:10.1016/j.jinsphys.2010.04.011
  5. Calas-List D, Clare AJ, Komissarova A, Nielsen TA and Matheson T (2014) Motor inhibition affects the speed but not accuracy of aimed limb movements in an insect. Journal of Neuroscience 34: 7509 - 7521. doi: 10.1523/JNEUROSCI.2200-13.2014
  6. Gunderson P, McKnight A and Matheson T (2011) Functional recovery of aimed limb movements following partial amputation in the locust Schistocerca gregaria. Proceedings of the 33rd Göttingen Neurobiology Conference, T21-13A.
  7. Page KL, Zakotnik J, Dürr V and Matheson T (2008) The motor control of aimed limb movements in an insect. Journal of Neurophysiology 99: 484 - 499. DOI:10.1152/jn.00922.2007
  8. Rogers SM, Matheson T, Sasaki K, Kendrick K, Simpson SJ and Burrows M (2004) Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locusts. Journal of Experimental Biology 207: 3603-3617. DOI: 10.1242/jeb.01183
  9. Zakotnik J, Matheson T and Dürr V (2006) Co-contraction and passive forces facilitate load compensation of aimed limb movements. Journal of Neuroscience 26(19): 4995-5007. DOI: 10.1523/JNEUROSCI.0161-06.2006

Relevance to BBSRC and Approvals

BBSRC Strategic Research Priority: Molecules, cells and systems

Techniques that will be undertaken during the project:

  • Techniques in the discipline of Biology
    • In vivo electrophysiology
    • Muscle force measurements
    • Limb kinematics
    • Animal behaviour
  • Techniques in the discipline of Biomechanics and Engineering
    • Micro-CT (X-ray micro-computed tomography)
    • Finite Element Analysis
    • Biomechanical modelling
Contact: Dr Tom Matheson, University of Leicester