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Neuromechanical Coupling in the Regulation of Muscle Tone and Joint Stiffness

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Neuromechanical Coupling in the Regulation of Muscle Tone and Joint Stiffness Scand J Med Sci Sports 2014: ••: ••–•• © 2014 John Wiley & Sons A/S. doi: 10.1111/sms.12181 Published by John Wiley & Sons Ltd Review Neuromechanical coupling in the regulation of muscle tone and joint stiffness A. R. Needle, J. Baumeister, T. W. Kaminski, J. S. Higginson, W. B. Farquhar, C. B. Swanik Department of Health and Exercise Science, Appalachian State University, Boone, North Carolina, USA Corresponding author: Alan R. Needle, PhD, ATC, CSCS, Holmes Convocation Center 011, 111 Rivers St., ASU Box 32071, Boone, NC 28608, USA. Tel: 828-262-4039, Fax: 828-262-3138, E-mail: [email protected] Accepted for publication 23 December 2013 The ability of the nervous system to accommodate outcomes, although research using proprioceptive tasks changes to joint mechanics is crucial in the maintenance and quantifying reaction times has led to equivocal of joint stability and the prevention of injury. This results. Recent innovations have allowed for the simulta- neuromechanical coupling is achieved through several neous measurement of mechanical and nervous system mechanisms such as the central and peripheral regulation function among these subsets. The intent of this review of muscle tone and subsequent alterations to joint stiff- was to explore the relationships between joint stiffness ness. Following joint injury, such as a ligamentous and nervous system function, and how it changes follow- sprains, some patients develop functional instability or ing injury. By better understanding these mechanisms, require surgery to stabilize the joint, while others are able researchers and clinicians may better develop and imple- to cope and display limited impairments. Several ment rehabilitation protocols to target individual deficits researchers have attempted to explain these divergent among injured populations. The maintenance of joint stability is a critical factor of decerebrate felines (Bosma & Gellhorn, 1947; Eccles for daily function and the prevention of falls and injury. & Lundberg, 1959; Burke, 1983; Sinkjaer, 1997; Throughout physical activity, the neurological and Breakefield et al., 2008). However, limited research mechanical components of a joint must work collec- exists regarding potential mechanisms capable of alter- tively to both prepare for and react to injurious pertur- ing this descending drive among healthy adults, as well bations (Sherrington, 1911; Freeman & Wyke, 1967; as those with joint injury. This information would be Lacroix, 1981; Sinkjaer et al., 1988; Johansson et al., clinically useful because tone may be described as the 1991). The result of this neuromechanical coupling is a muscles’ “state of readiness,” which can be modified modulation in muscle tone that can optimize joint stiff- based on specific functional tasks and the individual’s ness for specific tasks, contributing toward injury pre- level of anxiety (Saper, 2000; Davis et al., 2011). There- vention and improved functional performance (Sinkjaer fore, the neuromechanical properties of muscle tone et al., 1988; Nielsen et al., 1994). The intent of this have an important role for both maximizing functional article is to examine the combined influence of muscle performance and preventing injury. tone and joint stiffness regulation with specific consid- eration to their roles in sports medicine practice. Peripheral mechanisms Muscle tone Original theories suggested that muscle tone is mediated peripherally by the fusimotor system – the neural circuits The phenomenon of muscle tone is a commonly misun- existing between the muscle spindle, its afferent axons derstood concept when discussing injury prevention and (Type Ia & Type II) and the gamma (γ) motor neurons athletic performance (Masi & Hannon, 2008). Defined as that act to alter spindle sensitivity by changing the length the low-level steady-state muscle contraction at rest, it and tension of intrafusal fibers (Burke, 1983; Johansson exists unconsciously, and controls the tautness of a et al., 1986; Bergenheim et al., 1995; Pearson & Gordon, relaxed muscle. Upon passive stretching of muscles with 2000). This increase, or gain in the gamma motor neuron heightened tone, the mechanical response will be drive is associated with coactivation of the alpha motor increased resistance to length changes (Davidoff, 1992). neurons controlling the contraction of the extrafusal Much of what we understand about muscle tone relates skeletal muscle fibers (Johansson et al., 1986; Knutson, to pathological populations including forms of hyperto- 2000). Therefore, increased activity of the fusimotor nicity such as spasticity and rigidity; or in vitro models system translates into higher levels of resting skeletal 1 Needle et al. Table 1. Classification and conditions affecting muscle tone Condition Description Potential Cause(s) Hypotonicity Abnormal decrease in muscle tone; associated with hypoactive Lower motor neuron lesions reflexes Posterior cerebellar lobe lesions Hypertonicity Abnormal increase in muscle tone with resistance to active and Upper motor neuron lesions passive movement; associated with hyperactive reflexes Anterior cerebella lobe lesions Rigidity Hypertonicity to muscles on both sides of a joint Parkinson’s disease and other neurological disorders Spasticity Hypertonicity on one side of a joint Spinal cord injury above T12, head injury, cerebrovascular accident, cerebral palsy Clonus Uncontrolled oscillation of muscle in a spastic muscle group Upper motor neuron lesions Dystonia Involuntary muscle contraction and abnormal posture in a specific Task-specific part of the body Interruption of cortical-basal ganglia loops. Adapted from: Gutman, S.A. 2001, Quick Reference Neuroscience for Rehabilitation Professionals, 1st edition, Slack, Inc., Thorofare, NJ. muscle contraction or tone. When this reflexive loop connect tone to the muscles’ “state of readiness,” we becomes overactive, disorders of muscle tone such as should consider the process of events necessary for alter- spasticity and hyperreflexia may occur (Burke, 1983; ing tone from a resting, “baseline” state. Sinkjaer, 1997; Hallett, 1998; Breakefield et al., 2008; If the nervous system had to be “turned on,” such as Hall, 2011). However, this approach to understanding awaking from a deep sleep, the sequence for generating muscle tone is somewhat isolated to the peripheral muscle tone would proceed as such. The reticular for- nervous system (PNS), but it is known that altera- mation will emit excitatory signals to arouse the brain tions to the central nervous system (CNS) can lead to and trigger awareness across the cerebral cortex. Signals pathologies related to muscle tone (Table 1) (Bosma & originating in the brainstem and cerebellum will travel to Gellhorn, 1947; Eccles & Lundberg, 1959; Burke, the gamma motor neurons along extrapyramidal path- 1983). ways including the reticulospinal, vestibulospinal and rubrospinal tracts. Muscle tone will then begin to spread through extrapyramidal pathways that include the Central mechanisms reticulospinal, vestibulospinal and rubrospinal tracts Several central mechanisms have been associated with originating in the brainstem and cerebellum travelling to heightened muscle tone including pathways from the the gamma motor neurons (Moruzzi & Magoun, 1949; cerebellum, basal ganglia and thalamus (Burke, 1983; Siegel et al., 1983; Saper, 2000; Hall, 2011). This causes Saper, 2000; Hall, 2011). These structures are capable of the spindle to become taut, as if the muscle were sud- altering muscle spindle sensitivity by regulating inhibi- denly stretched, stimulating the intrafusal spindle tion to the fusimotor loop (Eccles & Lundberg, 1957). sensory organ. The intrafusal fibers generate an excit- Therefore, increased intracortical inhibitory activity is atory afferent signal that is transmitted back to the spinal responsible for decreasing muscle tone (Eccles & cord through fast sensory nerves. These sensory fibers Lundberg, 1957; Rymer et al., 1979; Ridding et al., directly synapse with α motor neurons, resulting in a 1995; Hallett, 1998). Much of what we know about this monosynaptic stretch reflex and contraction of the same relationship comes from observations among patients muscle containing the spindles (Pearson & Gordon, with CNS disorders that, for a variety of reasons, have 2000). Together, with signals from the corticospinal difficulty regulating inhibitory and excitatory signals tract, with modification by the basal ganglia, the alpha- within the CNS. This leads to an outward appearance gamma co-activation will establish baseline levels of of altered muscle tone, including spasticity and dysto- muscle tone (Burke, 1983). This would initially be medi- nia (Breakefield et al., 2008). Findings of decreased ated simply through the fusimotor loop; however, as this intracortical inhibition are consistently observed in process occurs, the anterior and posterior spinocerebellar spastic and dystonic populations, as well as increased tracts will transmit new proprioceptive information to motor excitability suggesting a loss of cortical mediation the cerebellum (Saper, 2000). The result leads to a where the excitatory pathways are left uninhibited, feedforward/feedback loop such that the cerebellum leading to continuous increased motor neuron firing modifies activity of the brainstem and basal ganglia to (Ridding et al., 1995; Devanne et al., 1997; Hallett, control tone (King, 1948; Saper, 2000; Hall, 2011). 1998). Because of these complex interrelationships Without inhibition from higher cortical structures, the among the
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