Chapter 6 Muscular Support of the Spine
Spinal muscles have long been ignored contributors to spine stability. Paraspinal muscles have been inadequately appreciated and regarded (“lift with your legs, not with your back”), incised with impunity, suffered injury from retraction, neglected through rest/traction, and denervated capriciously. Even in the early 21st century, when bone and collagenous tissue structures (ligaments, tendons, intervertebral discs) are targets of intense basic scientific study, information on spinal muscles often remains empirical, subjective, nonreproducible—and, at worst, harmful. Intended as a compendium of available information and inferences of function, this chapter should challenge the reader to preserve, restore, train, and study the spine.
Muscle, in general, is a highly plastic, adaptable organ. Muscles are classified into three broad categories—striated, smooth, and cardiac muscle—categories that have as much to do with their neurologic control as with their histologic appearance. For the most part, our understanding of muscle form and function is derived from an extensive study of muscles of the extremities. Spine muscles, on the other hand, have changed with each phylogenetic selection that produced vertebrates, mammals, and eventually Homo sapiens. Histologically, muscle form and function are preserved from other species, but spine muscles have importance in the human beyond that seen in other animals.
The muscles that act as the dynamic control mechanism of the spine constitute the largest collective, coordinated group of muscles in the human body. Human spinal muscle makes us unique among species, allowing us to walk upright exclusively—hence the further ability to carry items to a safe place and thus “accumulate excess.” The ability to acquire surplus allows for specialization within a societal structure, impelling the dominance of our species. Without fear of overstatement, our evolutionary success as a species owes everything to the unique structure and function of spinal muscle.
Muscle serves a defined (and seemingly paradoxical) purpose to simultaneously vitalize with movement and protect with strength the central neural communication link between the brain and periphery. In the past, mischaracterizations of the spine as an overrated “electrical conduit” protecting vital message transduction to the limbs have predominated. This disingenuous oversimplification ignores the fact that interactions with the environment, including force generation, dynamic control, proprioception, and balance, benefit from and often require the intricate coordination of spine function.
The dynamic structure of the spine relies upon muscle to animate with motion its series of paired joints and hydraulically pressurized discs. This dynamic control protects the neural elements while maximizing freedom of mobility. A muscle’s function is enhanced by the stability, afferent feedback, and proprioceptive information provided by its associated ligaments, tendons, and joint capsules.1 This unique combination of motion and stability is demonstrated by the human skill of manipulating objects near the ground from a bipedal stance to lift and carry them to another location. Arguably, the ability to accomplish this “everyday task” has been a key to our success as a species, because the ability to bend efficiently from the waist in combination with squatting and hunkering allows accrual of excess to ensure against environmental pressures like famine and drought. A stable “biomechanical chain” that transfers force efficiently from hands to arms, shoulder girdle, spine, pelvis, and legs and to a stable foot base is essential. In this functional example, the spine musculature acts as a dynamic stabilizer of the biomechanical chain in several ways. It is here that one should recall Panjabi’s description of the interplay of the three subsystems of spinal control: muscle control, passive-restraint control, and neural control.2–4 The cotensioning of abdominal muscles at a distance (force multiplied by a lever arm to generate moment or torque) combined with the collective dorsal force of the erector spinae muscles during flexion-extension allows maintenance of a “balance point.”5–7 At each individual motion segment, the interspinalis, multifidus, and, possibly, intertransverse muscles also provide stability through compressive force spanning only one motion segment.5,6,8,9 Coupled ventral and dorsal forces have a net compressive force that, in turn, balances motion at the instantaneous axis of rotation for each motion segment, thereby maintaining compression at the disc and minimizing angular change. This net muscle force serves to offset other forces, thereby maintaining the force vector perpendicular to the disc’s plane like the guy wires supporting a tent or flagpole or radio tower.10,11
In sum, muscles supply dynamic, as well as static, axial compression force to allow for maximal load bearing (for bipedal carrying/lifting) capacity while maintaining function with economy of energy output. Energy is economized via the following mechanical adaptations unique to human musculature: maintaining a balanced plumb line (not working against gravity to maintain posture) with three offsetting curves, sharing tension bands to distribute loads, coupling forces when motion is required, and distributing load/work among the other osteoligamentous static structures.12
As the father of American architecture, Louis Sullivan stated in 1896, “form ever follows function,” and this is true for the human form as for the American skyline. With this in mind, understanding spinal muscle cannot be complete without acknowledging the role of spine muscles in evolutionary change. Evolutionarily, it appears that the common ancestors of land-dwelling vertebrates (including mammals) were ocean-dwelling animals similar to today’s fish. Living in water, these animals had to contend with very different forces from creatures that live on land. Large paravertebral muscles provide lateral flexion-extension (crossing the sagittal plane) to propel their bodies through water—demonstrated by the lateral tail motion of the fish. This form of locomotion is evolutionarily conserved in amphibians and land reptiles (even with addition of limbs) as demonstrated by the lateral locomotion of species in the order Crocodylia, including the modern alligator or crocodile. Currently extant reptiles propel themselves forward using lateral spinal motion (side-winding). Propulsion is achieved by alternating contraction of spine muscles that in turn creates alternating sagittal convexities of the spine. This repetitive spine motion allows the ipsilateral foreleg to move forward while the contralateral hindfoot (on the concave side) is brought closer to the contralateral foreleg in preparation for the next reciprocal lateral movement that repeats the motion-event contralaterally.
Adaptation (the results of which are not observed in any reptiles alive today) resulted in a 90-degree transformation of spine muscle motion. This characteristic, seen almost universally in mammals (the platypus and echidna being exceptions), presumably provides an advantage during land locomotion, allowing for explosive growth of the class Mammalia. The transformation allows for flexion-extension (crossing the coronal plane) that enables a greater distance per stride (as seen with the horse or cheetah at full run). Interestingly, land mammals that subsequently repopulated the oceans (whales, seals, manatees) maintained their motion orientation through the coronal plane. This form of spinal locomotion resulted in the vertical orientation of the mammalian tail fluke (a 90-degree transformation compared with fish), even though adaptive pressure has resulted in changes to the other extremities that appear similar to fish.
From an evolutionary standpoint, motion is a balancing act. First, form is intended to maximize the functions of swiftly arriving at a food source or a potential mate while evading a predator. On the other hand, the demand for speed must be balanced with metabolic efficiency that allows the species to survive perturbations in the environment. As stated previously, controlling spine motion (like flexion) with muscles alone is inefficient. Moreover, the space required for the abdominal/thoracic contents further limits the potential size of spine muscles.13 The evolutionary solution is twofold: (1) strong, elastic dorsal spinal structures (midline ligaments, joint capsules, and lumbodorsal fascia) produce (a) passive restraint, particularly to lumbar spine flexion/extension, and allow (b) static “hanging on the ligaments” subject only to slight, plastic “creep,” but without muscular effort; and (2) a lever arm advantage from quadrupeds to use the dorsal pelvic muscles as simultaneous motors and stabilizers of lumbar extension and lower extremity abduction.14 Specifically, the gluteus and psoas muscles drive the legs more efficiently when the lumbar spine laterally flexes to provide a passive return of energy expended via reciprocal motion.15 This is of special importance with respect to lumbar and cervical lordosis during surgical procedures as well as in considering the length of construct: excessive fusion length and/or other violations of biomechanical principles lead to decreased efficiency and a painful, less functional patient. Finally, the interplay of the muscles with static structures for metabolic efficiency may have important though insufficiently studied implications for research into so-called motion-preserving technologies.
In summary, the combination of a dorsal ligamentous complex and powerful muscles of the buttocks and dorsal thighs (along with the psoas muscle contributing to controlling the degree of lordosis—discussed later) permits the spine to function like a crane. The boom is the ligament-stabilized flexed spine, the fulcrum is the hips, and the counterweight is the buttocks (maintaining pelvic position with respect to the femurs). Finally, the structure is vitalized by the pelvic extensor musculature that is analogous to the crane’s engine.16,17 This combination of passive and active restraint allows for metabolic parsimony. An important, experimentally observable economy of effort is the tendency of the spine to “hang off its ligaments.” This action is a position of comfort and a metabolic conservation frequently observed in stooped laborers and observable in most normal subjects tested. In other words, normal subjects monitored with surface electromyography preferentially flex forward to end range with the lumbar spine (to the point of myoelectrical silence) before adding the component of hip flexion during the initial act of lifting.18–20 Another efficiency created by muscle is the curvilinear structure of the spine. The combination of cervical lordosis, thoracic kyphosis, and lumbar lordosis creates a balance (and though not myolectrically “silent”) requiring minimal muscle output by utilizing the static structure of the thoracolumbar fascia during standing.12
The curvilinear structure of the spine that optimizes efficiency is also a prerequisite for human bipedal ambulation and stance. The lumbar lordotic curve converts lateral flexion to torque through the pelvis to the femurs. As noted earlier, this action economizes effort, with upright propulsion leading to a balanced human gait that would be difficult without lumbar lordosis. Conversely, ambulation without lumbar lordosis leads to the shuffling strides of the upright apes whose gait is clearly dissimilar to that of healthy humans (but similar to that of flat back surgical failures). Moreover, the curvilinear structure of the spine permits a greater load to be lifted and carried (so important in human evolution). Spine biomechanical research suggests that cocontraction of spinal and abdominal muscles is the primary generator of the curvilinear structure of the spine that enables greater load bearing than straight-spine models (1200 N vs. 100 N). Furthermore, instantaneous, axial-rotational forces between segments in straight-spine models may lead to rapid failure when the spine is progressively loaded.21
This model corroborates observational data of the dynamic contribution of spine muscles to the creation of a compressive-stabilizing force. The cumulative compressive forces applied by the action of muscle, tendon, ligament, and fascia to bony and disc structures enable the spine to withstand greater physiologic forces in sagittal motion as well. This model is analogous to taut guy wires allowing flimsy tent material to withstand 100-mph winds. Tension provided by intrinsic muscle tone and ligamentous passive tension is hypothesized (by the “follower-load” theory) to provide a stabilizing force (in at least the sagittal and coronal planes of motion when standing). This tension directs the force vector to achieve pure compression of the motion segment (which withstands this force largely via the hydraulic force resistance of the disc). The compressive force vector minimizes shear forces implicated as a leading cause of disc degeneration.10
Finally, the individual contributions of spine muscles can, alternatively, be seen in the context of function dictating form. Instead of viewing spinal musculature in isolation, one may develop an appreciation of the spinal musculature as an efficiently evolved functional unit, improved upon from earlier iterations, and linking all skeletal muscles to act as one functional unit. The cervicothoracic, shoulder girdle, and upper extremity units are linked by paravertebral, abdominal, buttock, pelvic floor, and hamstring muscles to exert specific force vectors that combine with gravity and the constraint of the passive structures to allow carrying and manipulation while simultaneously maintaining bipedal stance or ambulating. The spinal musculature is the crucial link in a complete biomechanical chain that allows lifting and carrying (of greater than one’s own body weight) by the upper extremities while maintaining stable ground contact to haul items out of harm’s way or to a safe location. This ability to carry and hoard excess in turn provides maximal evolutionary advantage in an environmental context. The fine balancing act of performance and metabolic economy can tip over into dysfunction when subtle extrinsic (trauma) and/or intrinsic (fear-avoidance) disruptions evolve into a feed-forward system of dysfunction. This concept is ably demonstrated by Panjabi’s hypothesis of chronic back pain:22
Sub-failure injuries of the ligaments and embedded mechanoreceptors . . . generate corrupted transducer signals, which lead to corrupted muscle response patterns produced by the neuromuscular control unit. Muscle coordination and individual muscle force characteristics, i.e., onset, magnitude, and shut-off, are disrupted. This results [sic] in abnormal stresses and strains in the ligaments, mechanoreceptors and muscles, and excessive loading of the facet joints . . . inherently poor healing of spinal ligaments, accelerate degeneration of disc and facet . . . over time, may lead to chronic back pain.
The relative resistance of muscles due to redundancy and overengineering belies a complex microstructure. Because muscle functions as the dynamic control mechanism of the skeletal system, its structural complexity allows the tissue to respond to environmental cues to be faster, stronger, or more metabolically parsimonious. This very adaptability has very likely made muscle an overlooked and underappreciated structure.
Muscle incorporates many long, overlapping cells specifically adapted for shortening. Voluntary, or skeletal, muscle is by far the most abundant (by volume) muscle type in humans. Muscles controlling spinal movement, in turn, constitute the largest assemblage of skeletal muscles in the body. Of the various muscle-specific organelles and matrix proteins, the most common constituents are actin and myosin isoforms, which represent approximately 25% to 30% of the total body protein synthesis.15,23 This net metabolic consumption underscores muscles’ complexity and versatility, which originates not in its chemistry but in its structure. Sarcomeres, the basic structural units (individual cells) of muscles, are attached end to end to form a muscle filament. Muscle filaments are grouped together in tight formation, with their respective nuclei and organelles pushed to the periphery to form myofibrils.24 Bathing the myofibrils, nuclei, and organelles is a fluid called sacroplasm whose fluctuating electrolyte concentration is controlled by the external, semipermiable lipid bilayer known as the sarcolemma. The myofibril architecture is highly organized, aligning longitudinally within the sarcolemma, which is indented by a motor axon at its myoneural junction. Myofibrils are bundled to form muscle fibers that are, in turn, covered and connected to other muscle fibers by an endomysium. The axial muscle fibers may be only a few millimeters in diameter but can be 5 cm or more in length. Many fibers are bound together by perimesium collagen to form organized fascicles that are bundled together to form what we call muscle.24,25 Muscle attaches to bone via a collagenous tissue called tendon. The function of this superstructure depends upon the two-way communication (between the alpha motor neuron and muscle and the Golgi-tendon complex and spinal reflex arc) and the variable neural innervation by one motor neuron that may coordinate contraction for anywhere from 15 to 5000 muscle fibers.
The rigidly organized substructure of the myofilament appears as light and dark striations under a light microscope—hence the designation striated muscle for skeletal muscle. Under normal circumstances, contraction of striated muscle does not occur without neural stimulus, whereas contraction of cardiac and most smooth muscle fibers autopropagates, triggering adjacent fibers to contract without neural stimulation. The cellular mechanics of contractions are relatively simple: actin filaments (occupying the light-colored I band at rest) slide over the myosin filaments (found in the A band and interdigitating with the I band at rest) until, with complete contraction, they completely overlap and eliminate the light H band under microscopic visualization. The biochemical reactions are more complex. Contraction initiates with the release of acetylcholine at the myoneural junction, depolarizing the sarcolemma by changing its permeability to sodium and potassium ions. The sarcolemma-induced ion cascade stimulates release of calcium ions, sequestered in the sarcoplasmic reticulum. These calcium ions bind the troponin complex (C, T, and I), inducing a conformational change that uncovers a “sticky” portion of the actin filament. Myosin, fueled by adenosine phosphate molecules (ATP and ADP), binds and unbinds actin to induce the ratcheting of the myosin along the length of the actin filament. The acetylcholine is rapidly hydrolyzed by acetylcholine esterase, and the calcium is rapidly sequestered back into the sarcoplasmic reticulum so that each nerve firing in skeletal muscle is a discrete, pulsed event rather than a sustained spasm. In this way, multiple stimulations of billions of sarcomeres induce the movements we see that form the basis of dynamic control.
When broken down to its constituent biomechanical parts, it appears that the rate-limiting steps to muscle function are myoneural junction integrity, ionic stability, filament cohesion, and energy. On a more holistic scale, series elasticity, motivation, training, endurance, and energy supply become the rate-determining steps of muscle function. Discrete, independent control of muscle fibers (e.g., only a few motor units contracting or muscle control by multiple motor neurons) permits a gradation of contraction that enables—depending on circumstance—voluntary vacillation between refined control or rapid, maximal contraction. The strength of a single contraction, or “twitch,” depends on the number of fibers that contract. The ability to sustain the contraction (endurance) depends on the ability to recruit more muscle fibers with increasingly repeated firing frequency so that just enough fibers are recruited to do the minimum necessary to complete a task (muscle efficiency). Other factors, muscle fiber type or fuel source, may independently affect endurance (ability to sustain a contraction), but recruitment adapts through training and neurocognitive, motivational factors.
The fuel for muscle contraction (as well as for most bodily functions) is phosphate from the disassociation of adenosine triphosphate (ATP) to adenosine diphosphate (ADP). How the ATP is derived and the cost associated with fuel manufacture pays the salary of many professionals (and continues to propel an illicit subculture of pseudoscientists in medicine and nutrition). For the scope of this chapter, the major consideration is whether ATP is produced via hydrolysis of glucose into water and carbon dioxide or via the citric acid cycle (Krebs cycle). The implication of emerging research is that exercise may stimulate a more favorable milieu for local and distant cells through a paracrine effect. Lactic acid, when it accrues in “anaerobic” metabolism, is one of the implicated protein-signaling molecules.
As we go to press, the implications of new basic scientific research in muscle metabolism have not seen wide application in clinical care. Research based on the experimental work of George Brooks, termed lactate shuttle theory, suggests that higher concentrations of lactic acid produced in the skeletal muscles have beneficial local and possibly distant paracrine effects.26–28 This growing body of research implies that instead of being a “dead-end metabolite” or mediator of muscle fatigue (as was widely published in the 1960s through the 1980s), lactate may be the mediator of beneficial effects seen empirically in training and exercise. Some research even refutes the implication of lactic acid in fatigue and notes that pH effects of hydrogen ion excess are the primary agents of diminished contractile power.27 In total, the lactate ion may serve multiple beneficial roles in stimulating change in body milieu in the presence of muscle exertion to maintain constant energy (via conversion of lactate to glycogen); to recruit new energy sources (gluconeogenesis); to stimulate new vascularity (angiogenesis); and to promote a local cascade of healing, plasticity, and hyperplasia.26,29 Although it is beyond the scope of this chapter, there is an urgent need for research into this area because the raison d’être of spine physicians is based on activity, strength, and maintaining function after the patient leaves our office.
There are several ways to infer how the microstructure we have described influences the function of a healthy spine. Some analysis has focused on structural composition, enumerating the relative contribution of fiber length, fiber size, and fiber directional orientation to classify muscle. This modeling of physiologic cross-sectional area is combined with geometric calculations from the fulcrum (moment arm) to model idealized function and classify muscle type. Alternatively, the ATPase work of Engel in 1962 initiated a body of research demonstrating distinctly different motor units within skeletal muscle.30 Myotype classification schemes have proliferated based on histology, morphology, or function. Briefly stated, the interaction between the type of myosin heavy chain (ATP-binding site) and actin within individual sarcomeres determines functional differences based on this classification. Furthermore, the rate at which the myosin heavy chains can repetitively bind ATP and release ADP under conditions of physiologic stress defines the function of the sarcomere into one of three broad functional categories.31 Type I fibers have a slower twitch response (rate or frequency of a single contraction), with good fatigue resistance and lower tension development (power). Type II muscle displays a fast twitch, with broader recruitment for more forceful tension development, but relatively poor endurance as compared with type I muscle fibers. Type II fibers are often subdivided into type IIA (that still show a fast twitch response, but have a fatigue threshold between type I and type IIB) and type IIB, showing the fastest speed, the greatest recruitment force (power), and the most precipitous onset of fatigue.32,33 Though researchers continue to further subclassify fiber types, type I, type IIA, and type IIB muscles remain the basis of the broadest functional class of voluntary skeletal muscles. Structurally, type I fibers have rich capillary beds with high concentrations of mitochondrial enzymes and relatively low concentrations of glycogen and myosin adenosine triphosphatase—making them appear ideally suited for resisting fatigue associated with aerobic activity. The milieu of type II muscles is very different, with high concentrations of glycogen and a ready supply of ATP for fast, strong contractions in a fixed time period. It should be remembered that in gross structure, each muscle is a heterogeneous, woven tapestry consisting of all of the above fiber subtypes. Relative predominance of one particular fiber type is largely based on genetics and anatomic location of a particular muscle. However, one cannot forget the plasticity inherent in muscle and the mutability based on environmental factors of muscle, age of the individual, nutrition, training, demand, and type of exercise.34,35
In addition to muscle substructural form, there is also the distance from the joint’s axis of rotation. In a simple model, this distance is termed the lever arm or, more correctly, the moment arm. In the case of only one muscle acting on a joint, the moment arm can be represented by the distance of a muscle’s action in relation to the joint’s axis of rotation. In other words, the amount of muscle shortening causes joint excursion through an arc. From this basic knowledge, it is easy to appreciate that even if a muscle is predominantly type II muscle and built for speed and power, it might not translate to rapid joint angular velocity if there is a large moment arm. Instead, in this scenario, the muscle’s activity would be generating high torque at lower angular velocity. The architectural superstructure adds another layer of complexity with multiple intrinsic and extrinsic muscles exerting force to maximize strength and minimize shear, while economizing metabolic expenditure.