Central mechanisms of muscle tone regulation: implications for pain and performance

Abstract

Muscle tone represents a foundational property of the motor system with the potential to impact musculoskeletal pain and motor performance. Muscle tone is involuntary, dynamically adaptive, interconnected across the body, sensitive to postural demands, and distinct from voluntary control. Research has historically focused on pathological tone, peripheral regulation, and contributions from passive tissues, without consideration of the neural regulation of active tone and its consequences, particularly for neurologically healthy individuals. Indeed, simplistic models based on the stretch reflex, which neglect the central regulation of tone, are still perpetuated today. Recent advances regarding tone are dispersed across different literatures, including animal physiology, pain science, motor control, neurology, and child development. This paper brings together diverse areas of research to construct a conceptual model of the neuroscience underlying active muscle tone. It highlights how multiple tonic drive networks tune the excitability of complex spinal feedback circuits in concert with various sources of sensory feedback and in relation to postural demands, gravity, and arousal levels. The paper also reveals how tonic muscle activity and excitability are disrupted in people with musculoskeletal pain and how tone disorders can lead to marked pain and motor impairment. The paper presents evidence that integrative somatic methods address the central regulation of tone and discusses potential mechanisms and implications for tone rehabilitation to improve pain and performance.

Keywords: complimentary and integrative health; movement coordination; muscle tone; musculoskeletal pain; neurophysiology; postural tone; stiffness.

Figure 1

Resting and postural tone. (A) Resting tone is assessed with the subject fully supported and is largely passive except for axial and proximal muscles. Postural tone is assessed during active postural maintainence. Resting and postural tone likely share mechanisims, however postural tone has a greater active component that prevents postural collapse. Note that the fraction between passive and active muscle tone depicted is only illustratve and depends on the specific muscle and postural context. (B) The involuntary tonic muscle activity during stance constitutes tone but holding a fist does not, because of the voluntary origin of the tonic contraction.

Figure 2

Neural circuitry underlying muscle tone. (A) Descending brainstem and supraspinal circuitry. Pontomedullary nuclei (PM tone nuclei) provide parallel descending tonic drive to the spinal cord to activate and modulate the excitability of spinal circuits through reticulospinal, vestibulospinal, and monoaminergic tracts. Solid and dashed lines indicate central and afferent projections, respectively. Pontomedullary tone nuclei include tone-excitatory regions in the ventral medullary reticular formation (vR), tone-inhibitory regions in the dorsal medullary reticular formation (dR), excitatory projections from the vestibular nuclei (VN), and two groups of monoaminergic nuclei: the noradrenergic locus coeruleus (LC), and serotonergic raphe nuclei (RN). The raphe nuclei are subdivided into caudal nuclei, which send descending projections to the spinal cord, and rostral raphe nuclei, which send ascending projections to the forebrain. Descending projections from the vR and dR also branch to co-regulate sympathetic nervous system activity. The monoaminergic tracts release noradrenaline (NA) and serotonin (5HT) onto motoneurons and diffusely across the spinal cord. The pontomedullary tone nuclei receive inputs from higher level structures, including the cerebral cortex, basal ganglia (BG), cerebellum (CB) and midbrain (MB), which includes the pedunculopontine nucleus, cuneiform nucleus, and periaqueductal gray. The neural integrators for the neck (NI) are also located in the midbrain and project to neck motoneurons. Note that known interconnections, for example those between the pontomedullary nuclei, are omitted for clarity. (B) Feedback circuitry in the spinal cord. Spinal cord feedback circuits are capable of adapting tone to postural demands; however, they require tonic excitation to function. These circuits consist of heterogeneous populations of interneurons (white ovals) distributed across spinal cord laminae. These interneurons differentially receive input from 1a stretch receptors and 1b tendon organs from ipsi-and contralateral limbs, respond to different stimuli, and project to motoneurons (black ovals). (C) Flexor and extensor muscles. The reticulospinal and monoamine tracts project to both flexors and extensors, while the vestibulospinal tract projects solely to extensors. Note that while only a pair of muscles are shown, muscle tone is broadly distributed across the musculature and thus involves activation throughout the spinal cord.

Figure 3

Mechanical and neurological influence of muscle tone on performance and pain. Postural tone creates a distributed network of stiffness and resistance (i.e., “postural frame”) that can mechanically affect movement coordination and musculoskeletal pain. Tone can also exert its influence neurologically, through changes in excitability, which may influence performance and pain through the resulting changes in neural responses.

Figure 4

Multifactorial influences on muscle tone.

Figure 5

Model of intervention pathways for muscle tone. Tone can be influenced through a diverse combination of pathways, which likely underlie differences in the distribution, adaptivity, and interaction across the body. For instance, vibration changes tone through serotoninergic pathways from caudal raphe nuclei (RN), while attention and static motor imagery involve the cortex and likely also tonic reticulospinal pathways (vR, dR). Effects of vigilance and arousal on tone are mediated through the locus coeruleus (LC), and movement affects tone though RN, both of which influence overall motor gain. Movement also affects tone through neural integrators (NI), which set tone levels after a movement, and have been located for the neck in the midbrain. Head orientation and neck posture affect tone through the vestibular nuclei (VN). Haptic touch could influence tone via loops through the brainstem, cerebellum and cortex. In contrast, stretching is likely to alter tone locally though spinal cord circuitry. Note that this diagram is meant to illustrate the diversity of potential pathways and not to be exhaustive.