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Role of the Reticulospinal and Corticoreticular Systems for the Control of Reaching In Role of the Reticulospinal and Corticoreticular Systems for the Control of Reaching in Non Human Primates. DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Lynnette Ruth Montgomery Graduate Program in Neuroscience The Ohio State University 2013 Dissertation Committee: John Buford. Advisor Lyn Jakeman Susan Travers D. Michele Basso Copyrighted by Lynnette Ruth Montgomery 2013 Abstract The control of reaching involves an interplay of multiple motor systems within the central nervous system entailing the use of both upper limbs (UL) and the upper trunk. The purpose of this dissertation was to describe how two of these motor systems (corticospinal and reticulospinal) contribute to the control of reaching. Firstly, we detailed the organization of reticulospinal cells within the pontomedullary reticular formation (PMRF) that project to the primate cervical enlargement in the primate cervical spinal cord. Secondly, we investigated the effects that three cortical motor areas have on both ipsilateral and contralateral motor output. Thirdly, we described the nature and organization of projections from the supplementary motor area (SMA) to the PMRF and specifically to reticulospinal cells that project to the cervical enlargement in the primate. The reticulospinal system, which originates from the PMRF in the brainstem, has been shown to contribute to the control of reaching through its influence on muscles of the trunk and proximal UL. Not only is this system focused on more proximal musculature, but it is also a bilateral system, meaning that motor outputs can influence both UL’s. Despite this potential role in the control of skilled UL movement, there are currently few details in the literature regarding the structural organization of the reticulospinal system in the primate. Using retrograde tract-tracers injected into the cervical enlargement of non-human primates (Macaca fascicularis), we labeled ii reticulospinal cells that projected to the cervical enlargement where alpha motoneurons for UL muscles are located. Following unilateral tracer injections, we found that reticulospinal cells from both the left and right PMRF project to the cervical enlargement, however significantly more cells were in the PMRF ipsilateral to the injection site. Most reticulospinal cells were in the nucleus reticularis pontis caudalis (PnC) and the rostral portion of the nucleus reticularis gigantocellularis (Gi); this was also where the majority of the largest cells were located. Although there are multiple motor systems involved in the control of reaching, the corticospinal system has received the most attention due to the fact that – (1) projections originate directly from the motor cortex, (2) this system is most developed in higher order animals such as non-human primates and humans, and (3) this system is particularly important for fine motor control in primates. Because the majority of corticospinal projections are contralateral in nature, studies have focused on its role in the control of the distal contralateral UL and few studies have investigated the role that the corticospinal tract plays in the control of the ipsilateral UL, and there is also a paucity of information about corticospinal control over proximal muscles in the UL and trunk. The second study in this dissertation uses electrophysiology - intracortical microstimulation and electromyography (EMG) - to investigate the contributions that the primary motor cortex (M1), SMA, and dorsal premotor area (PMd) make to the control of the ipsilateral and contralateral UL during a reaching task. These three areas were chosen because they are the site of the majority of corticospinal cells. Stimulus trains (36 biphasic pulses, 330 Hz) were delivered to one of these three cortical areas and EMG was recorded from iii select muscles in the upper trunk and proximal UL’s. Our findings showed that there were a number of muscle responses detected in the ipsilateral UL following SMA stimulation, especially around the trunk and shoulder girdle. Our use of stimulus trains meant that both direct and indirect motor pathways were activated. With this in mind, the fact that the onset of ipsilateral responses was delayed compared to the most direct contralateral responses following M1 stimulation indicated that ipsilateral responses were elicited through indirect pathways such as the reticulospinal pathway. As SMA produced a number of ipsilateral responses which seemed to be elicited through indirect rather than direct motor pathways, and the reticulospinal system in the primate projects primarily ipsilaterally to the cervical spinal cord in the primate, we wanted to detail whether a pathway existed between SMA, reticulospinal cells, and the cervical enlargement. Using neuroanatomical tract-tracers (anterograde tracers in SMA and retrograde tracers in the cervical cord), we identified labeled corticoreticular boutons in the ipsilateral and contralateral PMRF on fibers that originated from the arm representation of SMA. A small but significant number of these boutons came within 5 µM of labeled reticulospinal cells, making it likely that these boutons were making contact with these reticulospinal cells. Staining with a presynaptic marker (synaptophysin) provided further evidence that these boutons that came within 5 µM were forming functional contacts with reticulospinal cells. Although these contacting boutons were found in both sides of the PMRF, the majority of them were located in the PMRF ipsilateral to the SMA injection. The majority of these boutons were also located in PnC and rostral Gi where most of the reticulospinal cells are located. iv Thus, this dissertation presents evidence that the reticulospinal system in the primate is a bilateral, although predominantly ipsilateral pathway that projects to the cervical enlargement. We also provide evidence that premotor areas of the cortex, especially SMA, elicit a number of responses in the ipsilateral UL mainly proximal muscles of the trunk and shoulder girdle, and these responses appear to be elicited through indirect polysynaptic pathways. One such pathway that may be involved in producing these effects involves projections from SMA to reticulospinal cells, which then project to the cervical cord. With our final experiment we have provided evidence that such a corticoreticulospinal pathway from SMA to the cervical cord via the reticulospinal system does exist in the primate. This pathway is bilateral, although it is predominantly ipsilateral. This corticoreticulospinal pathway has the capacity to influence both ipsilateral and contralateral UL musculature and may provide a mechanism by which UL motor recovery can take place following cortical injury. v Acknowledgments I would like to thank my PhD advisor, Dr John Buford, for all of his guidance and support during this PhD experience. I would also like to offer a special thank you to Dr Lyn Jakeman who taught me invaluable skills in the area of neuroanatomy and general science. You have allowed me to be able to take my love and passion for neuroanatomy and turn it into my career. That is a gift I can never repay. Thank you also to my other committee members, Dr Michele Basso and Dr Susan Travers, for providing constructive guidance and helping me to make it this far. A very special thank you also goes to Stephanie Moran and Rebecca Slattery. There are many things I have learnt from you that have helped me both personally and professionally. Without you two I would not have had the confidence to get to the finish line. Finally, but most importantly, I would like to thank my family. To my husband, John, who has always been by my side and has always believed in me even when I did not believe in myself, I am eternally greatful for your support and love. To my mother, you taught me to always ask questions even when it is not the accepted thing to do and it is that drive which had driven me on to achieve the success that I have had. vi Vita 1993................................................................Graduated from Wavell Heights High 1999................................................................Bachelor of Physiotherapy, University of Queensland, Australia 2000-2001 ......................................................Physiotherapist, Royal Hobart Hospital 2002-2003 ......................................................Physical Therapist, Providence Everett Medical Center 2002-2003 ......................................................Per Diem Physical Therapist, Overlake Medical Center 2003-2005 ......................................................Physiotherapist, Palmerston North Hospital 2005-2007 ......................................................Physical Therapist, St Joseph’s Hospital and Medical Center 2007 to present ..............................................Graduate Research Associate, School of Health and Rehabilitation Sciences, The Ohio State University vii Publications Montgomery LR, Herbert WJ, and Buford JA (2013) Recruitment of ipsilateral and contralateral upper limb muscles following stimulation of the cortical motor areas in the monkey. Experimental Brain Research 230(2): 153-164. Fields of Study Major Field: Neuroscience viii Table of Contents Abstract ............................................................................................................................... ii Acknowledgments.............................................................................................................
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