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Perception, Perfusion & Posture

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Perception, Perfusion & Posture Perception, Perfusion & Posture Billy L Luu Ph.D. Thesis University of New South Wales 2010 THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: LUU First name: BILLY Other name/s: LIANG Abbreviation for degree as given in the University calendar: PhD School: MEDICAL SCIENCES Faculty: MEDICINE Title: PERCEPTION, PERFUSION & POSTURE Upright posture is a fundamental and critical human behaviour that places unique demands on the brain for motor and cardiovascular control. This thesis examines broad aspects of sensorimotor and cardiovascular function to examine their interdependence, with particular emphasis on the physiological processes operating during standing. How we perceive the forces our muscles exert was investigated by contralateral weight matching in the upper limb. The muscles on one side were weakened to about half their strength by fatigue and by paralysis with curare. In two subjects with dense large-diameter neuropathy, fatigue made lifted objects feel twice as heavy but in normal subjects it made objects feel lighter. Complete paralysis and recovery to half strength also made lifted objects feel lighter. Taken together, these results show that although a signal within the brain is available, this is not how muscle force is normally perceived. Instead, we use a signal that is largely peripheral reafference, which includes a dominant contribution from muscle spindles. Unlike perception of force when lifting weights, it is shown that we perceive only about 15% of the force applied by the legs to balance the body when standing. A series of experiments show that half of the force is provided by passive mechanics and most of the active muscle force is produced by a sub- cortical motor drive that does not give rise to a sense of muscular force through central efference copy or reafference. In addition to feeding perceptual centres of the brain, an efference copy of the motor drive also feeds cardiovascular centres to generate a pressor response during volitional contractions, the effect of sub-cortical motor output on the central pressor response was determined. It is shown that the postural leg muscles depend strongly on their high perfusion pressure during orthostatic posture but because the motor drive from the balance system does not generate a central pressor response they do not receive the benefit of increased perfusion pressure to offset the loss of contractility as they fatigue. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). …………………………………………………………… ……………………………………..… ……….…………… Signature Witness Date The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: Acknowledgement Foremost, I would like to express my sincere gratitude to my supervisor Dr Richard Fitzpatrick for giving me the opportunity to undertake my Ph.D studies in his laboratory. His continuous support, encouragement, and guidance throughout my doctoral research has been invaluable in my development and understanding of the principles of scientific research. The experience of working in his laboratory has ingrained in me the desire to broaden my knowledge in all aspects of human physiology. He is a great friend and mentor. I sincerely thank Dr Jean-Sébastien Blouin for inviting me to spend time in his laboratory in Vancouver. He generously donated his time and expertise to teach me recording and analysis techniques that offered an insight into the technical aspects of scientific research. I am grateful to Dr Brian Day and Dr Jonathan Cole for providing the experimental data presented in my thesis on an extremely rare patient that has peripheral sensory loss. I would also like to thank my colleagues at Prince of Wales Medical Research Institute for their participation in my experiments and for creating a wonderful environment for learning. In particular, I would like to acknowledge the other members of my laboratory, Annie Butler and Rebecca St George, for their encouragement, insightful discussions, and for making this an enjoyable experience. To Mr Hilary Carter, I am grateful for the numerous pieces of equipment that were developed for my research. To my family, I thank them for their support and understanding throughout my studies and for their encouragment to pursue my interests in physiology. ORIGINALITY STATEMENT ‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’ ……………………………………………........... ……………………………........... Signed Date COPYRIGHT STATEMENT ‘I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International. I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright material; where permission has not been granted I have applied/will apply for a partial restriction of the digital copy of my thesis or dissertation.' ……………………………………………........... ……………………………........... Signed Date AUTHENTICITY STATEMENT ‘I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the conversion to digital format.’ ……………………………………………........... ……………………………........... Signed Date i Abstract Upright posture is a fundamental and critical human behaviour that places unique demands on the brain for motor and cardiovascular control. This thesis examines broad aspects of sensorimotor and cardiovascular function to examine their interdependence, with particular emphasis on the physiological processes operating during standing. How we perceive the forces our muscles exert was investigated by contralateral weight matching in the upper limb. The muscles on one side were weakened to about half their strength by fatigue and by paralysis with curare. In two subjects with dense large-diameter neuropathy, fatigue made lifted objects feel twice as heavy but in normal subjects it made objects feel lighter. Complete paralysis and recovery to half strength also made lifted objects feel lighter. Taken together, these results show that although a signal within the brain is available, this is not how muscle force is normally perceived. Instead, we use a signal that is largely peripheral reafference, which includes a dominant contribution from muscle spindles. Unlike perception of force when lifting weights, it is shown that we perceive only about 15% of the force applied by the legs to balance the body when standing. A series of experiments show that half of the force is provided by passive mechanics and most of the active muscle force is produced by a sub-cortical motor drive that does not give rise to a sense of muscular force through central efference copy or reafference. In addition to feeding perceptual centres of the brain, an efference copy of the motor drive also feeds cardiovascular centres to generate a pressor response during volitional contractions, the effect of sub-cortical motor output on the central pressor response was determined. It is shown that the postural leg muscles depend strongly on their high perfusion pressure during orthostatic posture but because the motor drive from the balance system does not generate a central pressor response they do not receive the benefit of increased perfusion pressure to offset the loss of contractility as they fatigue. ii Contents Acknowledgement Originality, copyright and authenticity statements Abstract i Contents ii Preface iii Presentations from this thesis iv Chapter 1 Introduction: The physiology of human posture 1 Chapter 2 On the sense of force and weight 30 Chapter 3 The sensation of standing 51 Chapter 4 Perfusion and lower-limb muscle function 71 Chapter 5 Cardiovascular control during standing 91 Chapter 6 Conclusions and speculations 102 References 112 iii Preface This thesis brings together two broad areas of physiology to study how people stand. It focuses on the neural signals that control muscle and cardiovascular activities during human standing.
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