Task-dependent modulation of propriospinal inputs to human shoulder 

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Chapter 2. Review of Literature

Neural control of the proximal upper limb

An important function of the human upper limb is to transport the hand to a desired location in space. Goal-directed reaching relies upon coordination between the shoulder, elbow and wrist. Multiple neural centres, from brain to spinal cord, are activated to coordinate reaching tasks that demand proximal stability and distal dexterity. Within the brain, the primary motor cortex (M1) and secondary motor areas of the posterior parietal cortex (Filimon, Nelson, Huang, & Sereno, 2009; Koch et al., 2008), premotor cortex (Chouinard & Paus, 2006; Davare, Andres, Cosnard, Thonnard, & Olivier, 2006) and the cerebellum (Fortier, Kalaska, & Smith, 1989; Fortier, Smith, & Kalaska, 1993) plan, control and execute voluntary motor actions. Descending motor commands from M1 are conducted by the corticospinal tract to alpha motoneurons (αMNs) in the spinal cord. αMNs in turn, innervate the musculature required to execute the desired voluntary movements. M1 modulates descending drive to muscles according to their function, throughout the different phases of a reaching task. During upper limb reaching, gripping and lifting, corticomotor drive to proximal and distal muscles differs according to the role of the muscles and stage of the task (Lemon, Johansson, & Westling, 1995; Turton & Lemon, 1999). Furthermore, common M1 neural networks coordinate the timing of proximal and distal muscle recruitment during functional upper limb tasks (Gagne & Schneider, 2007, 2008). While the cortex, particularly M1, has an important hierarchical role in coordinating muscle activity across the limb during reaching, there are still many unanswered questions regarding this neural control. For example, how are muscles across the limb co-contracted in such precise temporal and spatial patterns for a given task? What is the role of ipsilateral M1 in proximal upper limb control? Is muscle co-ordination mediated at the level of the spinal cord in addition to M1?
There is still much research required to answer these, and many other questions concerning neural control of the complex movements required to transport and support the hand in space during upper limb tasks.

Muscle Synergies for upper limb reaching

The central nervous system organises task-specific motor control in the upper limb by forming muscle synergies (Latash, 2008). The Greek definition of the word synergy means ‘work together’. Muscle synergies solve two fundamental properties of coordinated reaching; reliable and repeatable task performance and the flexibility to respond to challenges from the external environment (Haggard, Hutchinson, & Stein, 1995; Todorov & Jordan, 2002). Using muscle synergies the workload of a task can be shared across all muscles involved in its execution. The contribution of each muscle is constantly fine-tuned in response to afferent feedback from the periphery, to ensure task performance is maintained in the face of changing external demands (Todorov & Jordan, 2002; Torres-Oviedo, Macpherson, & Ting, 2006). The mechanisms for how the central nervous system plans and scales muscle synergies for specific tasks are still largely unknown (Latash, 2008; Kargo & Nitz, 2003).
Muscle synergies for upper limb reaching are formed within the primary motor cortex. Studies in the non-human primate M1 have found electrical stimulation of individual cortical neurons evokes complex goal-orientated movements such as reaching and bringing the hand toward the mouth (Aflalo & Graziano, 2006, 2007; Graziano et al., 2005; Graziano, Taylor, & Moore, 2002). M1 neurons are organised into clusters according to their preferred direction of firing, in order to facilitate the functional co-contraction of task-associated muscles (Georgopoulos & Grillner, 1989; Graziano et al., 2002; Todorov, 2000). There is good evidence from experiments in non-human primates and cats (Georgopoulos & Grillner, 1989; Holdefer & Miller, 2002; Merchant, Naselaris, & Georgopoulos, 2008; Morrow, Pohlmeyer, & Miller, 2009; Stark et al., 2007), and in humans (Cowper-Smith, Lau, Helmick, Eskes, & Westwood, 2010; Eisenberg, Shmuelof, Vaadia, & Zohary, 2010) that the direction of limb trajectory dictates the firing patterns of corticomotor neurons within M1. In the cat motor cortex, overlapping proximal and distal muscle representations underpin the muscle recruitment necessary to reach with the forelimb (Donoghue, Leibovic, & Sanes, 1992; Meier, Aflalo, Kastner, & Graziano, 2008; Schneider, Devanne, Lavoie, & Capaday, 2002; Schneider, Zytnicki, & Capaday, 2001). A task-dependent increase in functional connectivity between M1 muscle representations also serves to facilitate the recruitment of these muscles into synergies (Capaday, 2004; Capaday, Devanne, Bertrand, & Lavoie, 1998; Holdefer & Miller, 2002; Schneider et al., 2002). In humans, transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (FMRI) have demonstrated similar overlapping M1 representations for muscles commonly co-activated during upper limb reaching or pointing tasks (Devanne et al., 2006; Melgari, Pasqualetti, Pauri, & Rossini, 2008; Tyc, Boyadjian, & Devanne, 2005; Yao, Chen, Carmona, & Dewald, 2009). Other experiments using TMS have demonstrated that functional connectivity between M1 muscle representations is task dependant (Capaday, 2004; Devanne, Cohen, Kouchtir-Devanne, & Capaday, 2002; McNamara et al., 2007). The strength of synaptic connections between M1 muscle representations is modulated by intracortical inhibition, which increases or decreases neural connectivity depending on task requirements (Devanne et al., 2002; Gagne & Schneider, 2007, 2008). For example, use-dependent shifts in the overlap of muscle representations were observed when healthy adults were required to learn a novel muscle synergy (McNamara et al., 2007). Repetitive co-contraction of two muscles in an unlikely functional combination increased connectivity between their M1 representations, and shifted their cortical location toward the most efficient site to recruit the novel muscle synergy (McNamara et al., 2007). Hence the primary motor cortex is integral to the formation of muscle synergies in the upper limb, and plasticity within M1 facilitates the learning of new functional synergies.
Underpinning the generation of muscle synergies in healthy adults is the selective facilitation and inhibition of agonist and antagonist muscles that shapes corticomotor output. To selectively facilitate an agonist muscle, intracortical inhibition over the cortical representations of prime movers is reduced (Stinear and Byblow, 2003). This increases descending corticomotor drive to the agonist prior to voluntary contraction (Reynolds & Ashby, 1999; Ridding, Taylor, & Rothwell, 1995). Alternatively, intracortical inhibition over M1 representations is increased to selectively inhibit corticomotor drive and suppress antagonist muscle activity (Byblow & Stinear, 2006; Sohn & Hallett, 2004; Stinear & Byblow, 2003). Modulation of intracortical excitability between muscle representations within M1 promotes the synergistic recruitment of proximal and distal muscles for upper limb reaching tasks and allows the central nervous system to rapidly alter the synergy pattern in response to changing task demands.
While cortical mechanisms play a significant role in the generation of muscle synergies, networks in the spinal cord are also important (Bizzi, Cheung, d’Avella, Saltiel, & Tresch, 2008; Tresch & Jarc, 2009; Tresch, Saltiel, & Bizzi, 1999). Descending commands from motor cortex may serve to select, activate and flexibly combine movement ‘building blocks’ or muscles synergies (Cheung et al., 2009; Tresch & Jarc, 2009). As discussed further below, muscle synergies are the end result of activity across multiple levels of the central nervous system, including the cerebral cortex and spinal cord (Bizzi et al., 2008; Kargo & Nitz, 2003; Latash, 2008; Latash, Gorniak, & Zatsiorsky, 2008; Tresch et al., 1999).

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Bilateral innervation of proximal muscles

It has long been known that 10-15% of descending projections from M1 project to αMNs of the ipsilateral proximal limb (Brinkman & Kuypers, 1973; Kuypers, 1964). The functional significance of these uncrossed pathways for human upper limb motor control became open to formal investigation with modern non-invasive stimulation techniques. In healthy adults the ipsilateral M1 is facilitated when performing skilled manipulations with one hand (Perez & Cohen, 2008; Sohn et al., 2003). Facilitation of ipsilateral M1 is most apparent during complex tasks and tasks involving the non-dominant hand (Chen et al., 1997; Gerloff et al., 1998; Hummel et al., 2003; Muellbacher et al., 2000; Verstynen et al., 2005). Ipsilateral M1 contributes to the coordination of muscle recruitment timing during gripping and lifting tasks (Davare et al., 2007). Ipsilateral M1 is also important in the acquisition of new motor skills with the hand, indicating a role in adaptive motor learning (Duque et al., 2008). The mechanisms underlying ipsilateral neural control of the upper limb are still uncertain. The current understanding for distal hand muscles is that the ipsilateral hemisphere helps to shape contralateral motor output by modulating the level of transcallosal inhibition (TCI) between homologous muscle representations (Davare et al., 2007; Perez & Cohen, 2008; Sohn et al., 2003). However, it is a fundamental proposal of this thesis that ipsilateral M1 can also directly influence motor control of the proximal upper limb by its ipsilateral descending projections to the spinal cord.
It is proposed that descending commands from ipsilateral M1 are integrated with those from contralateral M1 at a spinal pre-motoneuronal level. In this case, selective muscle facilitation and inhibition would be a function of the spinal cord, and would rely on balanced descending input from both cortical hemispheres. It is probable the ipsilateral hemisphere has a greater role in motor control for proximal, than distal muscles of the upper limb. This is because proximal muscles are innervated by both ipsilateral and contralateral descending projections from motor cortex (Brinkman & Kuypers, 1973; Kuypers, 1964), although there is also evidence for ipsilateral projections to distal muscles of the upper limb (Wassermann, Pascual-Leone et al. 1994; Ziemann, Ishii et al. 1999). These descending pathways involve both excitatory and inhibitory projections from the contralateral corticospinal and ipsilateral cortico-reticulospinal tracts. The majority of crossed fibres from the contralateral corticospinal tract project from M1 and descend in the posterior limb of the internal capsule (PLIC) to the brainstem and spinal cord (Fries, Danek, Scheidtmann, & Hamburger, 1993). By activation of αMNs and inhibitory interneurons at the spinal level, M1 can dictate motor control of the contralateral upper limb. From premotor cortex, white matter tracts descend in the anterior aspect of the PLIC (Fries et al., 1993). From there, fibres from premotor cortex and M1 terminate onto reticular neurons in the brainstem (Andrews, Knowles, & Hancock, 1973; Catsman-Berrevoets & Kuypers, 1976; Kably & Drew, 1998; Matsuyama & Drew, 1997). The reticulospinal tract descends in the spinal cord as separate inhibitory (dorsal column) and excitatory (medial column) tracts, terminating on medial motor nuclei in the anterior horn of the spinal cord to innervate axial and proximal limb αMNs (Brinkman & Kuypers, 1973; Engberg, Lundberg, & Ryall, 1968a, 1968b; Kuypers, 1964). In the cat and non-human primate reticulospinal projections converge onto propriospinal and other interneurons, as well as directly onto αMNs (Boudrias, McPherson, Frost, & Cheney, 2010; Brinkman & Kuypers, 1973; Illert, Jankowska, Lundberg, & Odutola, 1981; Illert, Lundberg, Padel, & Tanaka, 1978; Riddle, Edgley et al. 2009). Therefore, M1 and premotor cortex can fine-tune contralateral descending commands at the spinal cord level via the ipsilateral reticulospinal tract. Control by the premotor cortex over the inhibitory dorsal reticulospinal tract is particularly robust (Andrews et al., 1973), indicating the ipsilateral hemisphere may be important for modulation of descending inhibition reaching the spinal cord. Ipsilateral corticospinal projections would likely contribute to control over αMN excitability, however would not allow precise control over inhibitory circuits. A candidate neural network for integrating contralateral and ipsilateral excitatory and inhibitory descending inputs at the level of the spinal cord is the cervical propriospinal system.

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Cervical propriospinal system

The cervical propriospinal system is a disynaptic component of the corticospinal tract, dedicated to the control of forelimb reaching in the cat and non-human primate (Alstermark, Isa, Pettersson, & Sasaki, 2007; Lemon, 2008; Lemon & Griffiths, 2005). Experimental animal models have demonstrated that propriospinal neurons (PNs), located at C3-4 in the spinal cord, integrate descending commands from special populations of M1 neurons, with ascending peripheral feedback from forelimb muscle afferents (Alstermark et al., 2007). This dual neural control allows PNs to modulate αMN excitability according to task demands, and update descending commands just prior to their execution if necessary. Indirect evidence indicates there is a similar arrangement in man, where it has been suggested putative PNs generate muscle synergies for upper limb reaching (Pierrot-Deseilligny & Burke, 2005). Ipsilateral M1 may contribute to upper limb motor control by the modulation of PNs in the spinal cord. This is because in the non-human primate and the cat, PNs receive robust projections from the ipsilateral reticulospinal tract (Alstermark, Lundberg, & Sasaki, 1984c; Illert et al., 1981; Illert et al., 1978). The evidence supporting a cervical propriospinal system is presented for both animal and human experiments respectively. It should be borne in mind that the evidence for the cervical propriospinal system in humans is by necessity indirect.

Chapter 1. Introduction 
1.1. Why study upper limb control?
1.2. Overview of the dissertation
Chapter 2. Review of Literature .
2.1. Neural control of the proximal upper limb
2.2. Cervical propriospinal system
2.3. Deficits of proximal upper limb control after stroke
2.4. Non-invasive brain stimulation
Chapter 3. Overview of Experimental Objectives & Methodology 
3.1. Objectives
3.2. Hypotheses
3.3. Experimental techniques
3.4. Ethics and subject selection
3.5. Statistical analysis
Chapter 4. Task-dependent modulation of propriospinal inputs to human shoulder 
4.1. Abstract
4.2. Introduction
4.3. Methods
4.4. Data Analysis
4.5. Results
4.6. Discussion
Chapter 5. Task-dependent modulation of inputs to proximal upper limb following transcranial direct current stimulation of primary motor cortex
5.1. Abstract
5.2. Introduction
5.3. Methods
5.4. Data Analysis
5.5. Results
5.6. Discussion
Chapter 6. Theta burst stimulation of human primary motor cortex degrades selective muscle activation in the ipsilateral arm110
6.1. Abstract
6.2. Introduction
6.3. Methods
6.4. Data Analysis
6.5. Results
6.6. Discussion
Chapter 7. Cathodal transcranial direct current stimulation suppresses ipsilateral projections to presumed propriospinal neurons of the proximal upper limb 
7.1. Abstract
7.2. Introduction
7.3. Methods
7.4. Data Analysis
7.5. Results
7.6. Discussion
Chapter 8. Contralesional hemisphere control of the paretic upper limb following stroke 
8.1. Abstract
8.2. Introduction
8.3. Methods
8.4. Data Analysis
8.5. Results
8.6. Discussion
Chapter 9. Discussion and Future Research .
9.1. Discussion
9.2. Neurophysiological models
9.3. Limitations
9.4. Future Directions

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