Investigation of the Role of Skin and Muscle Receptors in Proprioception at the Ankle Joint in Humans by Catherine R. Lowrey A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Human Health and Nutritional Sciences Guelph, Ontario, Canada © Catherine Lowrey, 2012 ii ABSTRACT INVESTIGATION OF THE ROLE OF SKIN AND MUSCLE RECEPTORS IN PROPRIOCEPTION AT THE ANKLE JOINT IN HUMANS Catherine Rose Lowrey Advisor: University of Guelph, 2012 Professor L. R. Bent This thesis is an investigation of the role of skin and muscle receptors in proprioception at the ankle joint in humans. Somatosensory afferents provide the central nervous system with cues that code for movement and position of the segments, senses collectively known as proprioception. Intramuscular receptors, in particular muscle spindles, code for length and movement velocity of muscles surrounding a joint and therefore play an integral role in proprioception. The role of cutaneous receptors is less clear. When activated via skin stretch they create illusory movements of the limbs, and they are capable of responding to movements of the joints. To what extent these cues are utilized over and above input from muscle spindles remains unknown. In addition, there is evidence that cutaneous receptors may influence the sensitivity of muscle spindles by modulating their level of fusimotor activation. The aim of this thesis was to further examine the role of skin in proprioception and to determine whether or not skin of the foot and ankle is capable of modulating fusimotor drive to muscle spindles of the lower limb. The current thesis is comprised of three studies. The first experiment utilized a matching task at the ankle joint and determined that skin from the dorsum of the foot and ankle is necessary for accurate proprioception. The remaining two experiments used the technique of microneurography to record from single nerve afferents in awake, human participants. Initially, cutaneous afferents were isolated and recorded to determine the efficacy of using cooling over their receptive field as a method to decrease their sensitivity and output. Once cooling was established as an effective tool, the final experiment isolated and recorded from muscle spindles in response to passive, ramp and hold movements at the ankle. It was determined that a reduction in skin input (via cooling) altered the firing response of a portion of spindles. It is likely that this change in firing was due to modulation of fusimotor drive to the spindles. Collectively, the current work contributes the novel findings that skin on the dorsum of the foot is necessary for accurate proprioception at the ankle and that this is largely due to the role of skin as an independent proprioceptive channel. In addition, we have shown for the first time that a reduction in skin input from the foot dorsum is capable of modulating spindle discharge during a passive ramp and hold movement at the ankle, demonstrating a minor role for this interaction in proprioception. A secondary finding of the thesis was that cooling with ice is an effective tool for reducing input from all four classes of cutaneous mechanoreceptors. iii Acknowledgements I would like to thank my advisory committee, Dr. Leah Bent, Dr. Lori Vallis and Dr. Rich Staines for their continued guidance and support throughout the entire course of my Ph.D. and their invaluable contribution to the completion of this thesis. I would like to express heartfelt gratitude to my advisor Leah Bent. Thank you for inspiring in me a love of science and teaching me to always question. You are a wonderful mentor, an inspiring role model and a great friend. Thank you for providing me with the amazing and unforgettable experiences that I have had throughout the course of my Ph.D. Thank you to all of the research subjects who participated in this series of experiments and a huge thank you to my lab mates Andrew Woolnough, Nick Strzalkowski, Chris Lam, Stephanie Muise, Gaayathiri Jegatheeswaran, Adam Toth, Cale Templeton, Chris Hayes and everyone else from the lab, past and present. Thank you each individually for all your help, and for making the Neurophysiology lab the most insanely fun place to work. Special thanks to Nick for being my microneurography partner and for the invaluable help on all of my thesis projects. Finally I would like to thank my parents, my family and friends, and my husband Steve. This entire endeavor would not have been possible without all of your love and support throughout the years. For that, I am truly grateful. iv Table of Contents Abstract........................................................................................................................................................................ ii Acknowledgements..................................................................................................................................................... iii Table of Contents ........................................................................................................................................................ iv List of Tables .............................................................................................................................................................. vii Table of Figures ......................................................................................................................................................... viii CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .......................................................................................... 1 1.1 GENERAL INTRODUCTION ....................................................................................................................................... 1 1.1.1 Thesis synopsis ............................................................................................................................................ 1 1.1.2 Thesis overview ........................................................................................................................................... 4 1.2 SUMMARY OF GOALS OF THESIS .............................................................................................................................. 4 1.2.1 Testable Hypotheses ................................................................................................................................... 5 1.2.1.1 Experiment I ................................................................................................................................................. 5 1.2.1.2 Experiment II ................................................................................................................................................ 5 1.2.1.3 Experiment III ............................................................................................................................................... 6 1.3 STATEMENT OF ETHICS .......................................................................................................................................... 6 1.4 REVIEW OF THE LITERATURE ................................................................................................................................... 6 1.4.1 What is proprioception and why study it? .................................................................................................. 6 1.5 MUSCLE RECEPTORS: ............................................................................................................................................ 8 1.5.1 Anatomy of the muscle spindle ................................................................................................................... 8 1.5.2 Contribution to Proprioception ................................................................................................................... 9 1.5.3 Microneurographic Recordings of muscle spindle afferents: .................................................................... 11 1.5.3.1 Early Recordings ......................................................................................................................................... 11 1.5.3.2 Microneurographic recordings of afferent response to vibration ............................................................. 11 1.5.3.3 Passive muscle stretch ............................................................................................................................... 12 1.5.3.4 Active muscle stretch ................................................................................................................................. 13 1.5.3.5 Fusimotor control of muscle spindles ........................................................................................................ 14 1.5.3.6 How do spindle firing patterns result in the coding of movement? .......................................................... 16 1.6 CUTANEOUS RECEPTORS: ..................................................................................................................................... 18 1.6.1 Properties of Receptors and Afferents ...................................................................................................... 18 1.6.2 Adaptive properties of cutaneous sensory units ....................................................................................... 19 1.6.3 Structure and location of cutaneous receptors ......................................................................................... 20