J Electromyogr Kinesiol. 2012 (Oct); 22 (5): 785–794 ~ FULL TEXT
Joel G Pickar, DC PhD and Philip S Bolton, DC PhD
Palmer Center for Chiropractic Research,
Palmer College of Chiropractic,
Davenport, IA, USA.
Manually-applied movement and mobilization of body parts as a healing activity has been used for centuries. A relatively high velocity, low amplitude force applied to the vertebral column with therapeutic intent, referred to as spinal manipulative therapy (SMT), is one such activity. It is most commonly used by chiropractors, but other healthcare practitioners including osteopaths and physiotherapists also perform SMT. The mechanisms responsible for the therapeutic effects of SMT remain unclear. Early theories proposed that the nervous system mediates the effects of SMT. The goal of this article is to briefly update our knowledge regarding several physical characteristics of an applied SMT, and review what is known about the signaling characteristics of sensory neurons innervating the vertebral column in response to spinal manipulation. Based upon the experimental literature, we propose that SMT may produce a sustained change in the synaptic efficacy of central neurons by evoking a high frequency, bursting discharge from several types of dynamically-sensitive, mechanosensitive paraspinal primary afferent neurons.
From the FULL TEXT Article:
Manually-applied movement and mobilisation of body parts as a healing activity has been used for centuries (Wiese & Callender, 2005). A relatively high velocity, low amplitude force applied to the vertebral column with therapeutic intent, referred to as spinal manipulative therapy (SMT), is one such activity. It is most commonly used by chiropractors, but other healthcare practitioners including osteopaths and physiotherapists use it as well. Although SMT has been advocated for a wide range of health problems (Ernst & Gilbey, 2010), currently available best evidence suggests it has a therapeutic effect on people suffering some forms of acute neck and back pain particularly when it is used in combination with other therapies (Brønfort et al, 2004; Brønfort et al, 2010; Dagenais et al, 2010; Miller et al 2010; Walker et al 2010; Lau et al 2011). Its effect on chronic low back pain is less clear (Rubinstein et al 2011; Walker et al 2010).
SMT is typically applied when dysfunctional areas of the vertebral column are found. Clinicians identify these areas based upon palpatory changes in the texture and tone of paraspinal soft tissues, the ability to elicit pain and/or tenderness from these tissues, asymmetries in hard or soft tissue landmarks, and restrictions in spinal joint motion (Kuchers & Kappler 2002; Sportelli et al 2005). The clinician’s goal in applying a spinal manipulation is to restore normal motion and normalize physiology of the neuromusculoskeletal system in particular and potentially other physiological systems affected by the dysfunction.
The mechanisms responsible for the therapeutic effects of SMT remain unclear. Early theories proposed that the nervous system likely mediates the effects of SMT. For example, Korr (1975) proposed that SMT alters or modulates proprioceptive afferent input to the central nervous system. Twelve years later Gillette (1987) provided a speculative description of all afferent input likely to arise from SMT of the lumbar spine. The force-time profile of SMT, based upon the one study available at the time, was trapezoidal in shape, reaching a peak force of nearly 200N and lasting nearly 400ms before returning to pre-SMT levels. Identification of afferents likely activated by SMT was based upon a review of the experimental evidence describing the response characteristics of all known somatic mechanosensitive receptors to the mechanical features of the stimuli that activated them (eg, force magnitude, rate of force application). Much of the data concerning receptor-type and response characteristics were derived from studies involving the appendicular somatosensory system since little was known at the time about the axial somatosensory system. Consequently Gillette’s description (Gillette, 1987) provided a hypothetical profile of the afferent activity arising during SMT.
Since Gillette’s (1987) benchmark paper, considerably more is known about the morphology of the vertebral column’s somatosensory system (for example see Giles & Taylor 1987; Richmond et al 1988; Groen et al 1990; McLain 1994; Jiang et al 1995; Bolton 1998). Table 1 summarises receptor types that have been found in paravertebral tissues. Similarly, more is now known about the mechanical characteristics of SMT. Additionally, in vivo and cadaveric studies have better informed us about the kinematics of vertebral motion segments produced by SMT. Together these new data provide a more informed basis for modelling SMT activation of the axial somatosensory system.
This table lists the receptors that have been identified in paravertebral tissues of the Cervical (C), Thoracic (T), Lumbar (L), or Coccygeal (Cx) regions of the vertebral column using morphological (M) or physiological (P) studies. The species in which the respective receptors have been studies is listed together with one reference to a study involving the species and study type.
|Receptor||Region||Study Type||Species||Evidence (see for example)|
|Muscle Spindle||C||P||Cat||Richmond & Abrahams 1979|
| || ||M||Cat||Richmond & Bakker 1982|
| || ||M||Human||Boyd-Clarke et al 2002|
| ||C,T,L||M||Human||Amonoo-Kuofi 1983|
| ||L||P||Cat||Cao et al 2009|
|Golgi Tendon Organ||C||P||Cat||Richmond & Abrahams 1979|
| || ||M||Cat||Richmond & Abrahams 1982|
| || ||M||Human||Mendel et al 1992|
| ||L||M||Human||Roberts et al 1995|
| ||Cx||M||Bovine||Roberts et al 1995|
|Paciniform||C||M||Cat||Richmond & Abrahams 1982|
|Corpuscle|| ||M||Human||McLain 1994|
| ||L||M||Human Fetus||Jackson et al 1966|
| || ||M||Human||Jackson et al 1966|
| ||Cx||M||Bovine||Roberts et al 1995|
|Ruffini||L||M||Human||Roberts et al 1995|
|Ending|| || || ||Jiang et al 1995|
|Unencapsulated||C||M||Human||Mendel et al 1992|
|Nerve Endings||C,T,L||M||Monkey||Stilwell 1956|
| || ||M||Human Fetus||Groen et al 1990|
| ||L||M||Rat||Nakamura et al 1996|
| || ||M||Human Fetus||Jackson et al 1966|
| || ||M||Human||Jackson et al 1966|
The goals of this article are to briefly update our knowledge regarding several physical characteristics of an applied SMT and to review what is known about the signalling characteristics of sensory neurons innervating the vertebral column in response to spinal manipulation. Then based upon this data, we describe neurophysiological events that may contribute to the therapeutic effects of spinal manipulation.
PHYSICAL CHARACTERISTICS OF SMT
Mechanical parameters and forces associated with SMT
The biomechanical characteristics (i.e. force or displacement versus time curves) of a number of SMT techniques involving either manual or instrument-assisted protocols have been determined in studies performed directly on human subjects (for reviews see Lee et al, 2000; Herzog, 2010) or with the use of patient simulation devices (Kawchuk et al 2006; Graham et al, 2010). Figure 1 shows examples from both types of studies. As described by Herzog (2010), the profiles may be characterized by a pre-load phase, a thrust phase which rapidly rises to a peak force, and a resolution phase (see Fig. 1A).
Force time curves derived from high velocity, low amplitude spinal manipulation.
The characteristics of these profiles appear to vary depending upon region of the vertebral column to which they are applied (e.g., see Fig 1B). In human studies the kinematic parameters of SMT have been obtained using a flexible force-sensitive mat interposed between the clinician’s hands and the patient to record the force and duration of an SMT. SMT in the cervical region has relatively little pre-load ranging from 0 to 39.5N (Herzog et al 1993, Kawchuk et al 1992, Kawchuk & Herzog 1993). In contrast, the average pre-load forces during SMT in the thoracic region (139 N ± 46, SD) and sacroiliac region (mean 88N ± 78N) are substantially higher than in the cervical region and are potentially different from each other (Herzog et al, 1993). From the beginning of the thrust to end of the resolution phase, SMT duration varies between 90-120ms (mean = 102 ms). The time to peak force during the thrust phase ranges from 30-65ms (mean = 48 ms). Peak applied forces range from 99-140 N (mean = 118N, n= 6 treatments) (Herzog et al 1993). In the same study with SMT directed at the thoracic (T4) region and applied to three different patients by the same practitioner, the mean (± SD) time to peak force was 150 ms ± 77 ms and mean peak force reached 399N ± 119N. During the resolution phase, force returned to pre-SMT levels over durations up to 2 times longer than that of the thrust phase. When SMT was applied to the sacroiliac joint, mean applied peak forces reached 328 N ± 78N (Herzog et al 1993), with the thrust and resolution phases having similar durations (~100ms). The peak force during manipulation of the lumbar spine measured by Triano and Schultz (1997) tended to be higher than during the thoracic or sacroiliac manipulation measured by Herzog et al (1993) and the force-time profiles looked like half-sine waves with the time to and from peak taking approximately 200ms. Peak impulse forces during thoracic manipulation measured by Suter et al (1994) approximated the >400N peak impulse force measured by Triano and Schultz (1997).
The physical characteristics of an SMT may vary based upon the technique being used and the individual practitioner. While instrument assisted SMT may apply preload forces on the order of 20N, peak forces vary from approximately 50N to 380N depending on the instrument being used and selection of the instrument’s settings (Colloca et al 2005). Up to 38% of the instrument assisted thrusts were reported to produce absolute forces significantly different (P<0.05) from each other (Kawchuk et al 2006). In addition, the difference in applied force duration between 2 operators using instrument-assisted SMT can be as much as 75% (Kawchuk et al 2006). Similarly, measurements of SMT forces and displacements applied to a non-biological device simulating the SMT’s contact site also show variability. In a study measuring force and displacement over the duration of a Toggle Recoil SMT both force and displacement varied by 50% when performed by an individual practitioner while, between practitioners, force varied by up to 100% and displacement by up to 50% (Graham et al 2010). These findings presumably identify practitioner-related variability since neither the instruments nor the simulator’s mechanical properties change. During a non-instrument-assisted, predominately rotatory manipulative procedure applied to the neck, practitioners did not consistently perform the procedure in that peak thrust velocities were different. However, better inter-practitioner than intra-practitioner consistency was observed for thrust duration (Ngan et al 2005). Interestingly, a spinal mobilisation (low velocity) manual technique (cervical lateral glide) performed on the neck demonstrated very small intra-practitioner variability (Vicenzino et al, 1999).
It is clear that the mechanical parameters of SMT vary significantly depending on the manipulated region of the vertebral column, the type of procedure being performed, and characteristics of the individual practitioner. Nevertheless the force parameters are sufficiently described to allow modelling of the applied force to in vivo animal studies (see section below entitled STUDIES OF PARAVERTEBRAL SOMATOSENSORY AFFERENT ACTIVATION DURING SMT-LIKE MOTION).
Vertebral Motion with SMT
Less is known about the vertebral motion that occurs during SMT. Studies have been undertaken in unembalmed human cadavers to determine thoracic and lumbar vertebral motion induced by manual SMT. Absolute and relative linear (in mm) and angular (in degrees) vertebral motions have been studied in the thoracic spine (Gál et al 1997a, 1997b). Caudo-cranial and postero-anterior vertebral accelerations, and intra-intervertebral disc pressures have been studied in the lumbar spine (Maigne & Guillon, 2000). Although the number of subjects and datasets are small, these cadaveric studies indicate that vertebral kinematics following posterior to anterior thrusts involves biphasic and in some planes triphasic (pseudo-oscillatory) accelerations and rotations. Ianuzzi & Khalsa (2005a; 2005b) using an actuator to impose physiological rotations or simulated spinal manipulation loads to prosected human lumbar vertebral columns (T12-sacrum) investigated vertebral motion with 6 degrees of freedom. They demonstrated in the lumbar region that vertebral translation occurs primarily in the direction of the manipulative thrust and that vertebral rotations are relatively small (< 2°). Interestingly they also found that strain in the facet joint capsule did not vary either from side to side or between capsules of vertebrae adjacent to the vertebra receiving the thrust. From this, they hypothesized that mechanosensitive afferents in facet joint capsules both at the level of the applied thrust and at levels immediately adjacent would be activated.
Studies of vertebral motion associated with instrument-based SMT have been undertaken in anaesthetized humans (Keller et al 2003) and sheep (Colloca et al 2006; Keller et al 2006a, 2006b). More recently porcine prosected specimens of vertebral column were used to study vertebral motion (acceleration) occurring with instrument-induced SMT applied perpendicular and oblique to the SMT’s contact area (Kawchuk & Perle, 2009). Together these studies indicate that instrument-delivered SMT thrusts induce transient oscillatory (lasting 100-150ms), coupled (multiple axis) vertebral motions that vary depending on the subject being tested, and the location and magnitude of the applied force. The sheep preparation also demonstrates that, as might be expected, changing the force-time characteristics also changes the displacements and accelerations of both the target and adjacent vertebrae (Colloca et al 2006; Keller et al 2006a, 2006b).
STUDIES OF PARAVERTEBRAL SOMATOSENSORY
AFFERENT ACTIVATION DURING SMT-LIKE MOTION
Despite the significant ethical and technic al challenges, Colloca and colleagues performed electrophysiological recordings from the S1 nerve root and multifidus muscle in anaesthetised humans while simultaneously applying an instrument based SMT directed posterior to anterior in the lumbar region (Colloca et al, 2000, 2003; Keller et al 2003). For the nerve root, they reported the occurrence of electrical activity with a mean onset latency ranging from 8.2 to 10.7 ms following the thrust. For the multifidus muscle, they reported electromyographic activity (EMG) with a mean onset latency ranging from 5.5 to18.3 ms. While these studies indicate nerve and muscle activity may be modulated by a spinal manipulative thrust, they provide limited information regarding the type of neurons affected or the neurophysiological mechanisms involved.
Two quite different in-vivo experimental preparations using the anesthetized cat have been developed for investigating the neurophysiological effects of force-time or displacement-time profiles that simulate SMT when applied to the vertebral column. In one preparation defined angular motions can be imposed upon a cervical vertebra (Bolton & Holland, 1998). In the second preparation, defined loads can be applied to a lumbar vertebra under either force or displacement control (Pickar, 1999).
The first preparation has been used to emulate the force-time profile of an SMT’s thrust phase by imposing rotational displacements of the C2 vertebra about the neck’s longitudinal axis (Bolton & Holland 1998). Asymmetric tri-phasic (sine wave with dampened 2nd ½ cycle sine wave) displacements have also been used to emulate the acceleration profile and vertebral movements reported to occur during high velocity low amplitude thrusts in human cadavers (Gal et al, 1997a,b) and during instrument based spinal manipulation (Keller et al, 2003). Simultaneous with the rotational displacements, electrophysiological recordings from ipsilateral or contralateral projecting primary afferents have been made.
The second preparation utilizing a computer-driven, feedback motor was first used to emulate the force-time profile of high velocity low amplitude manipulations given by clinicians to the lumbar spine (Pickar & Wheeler, 2001). Loads were applied at the L6 spinous process (cat’s have 7 lumbar vertebrae) and directed cranially in the coronal plane using a ramp and hold (0.3s) force profile representing the manipulation’s pre-load phase followed by a force profile rising in 100ms to a peak load of 100% of the cat’s body weight representing the thrust phase. Simultaneously, electrophysiological recordings were obtained from individual primary afferents innervating the L6 paraspinal tissues. In subsequent experiments, manipulative loads have were applied to the L6 vertebra and directed ventrally in the transverse plane (Sung et al 2005; Pickar & Kang 2006; Pickar et al, 2007). Peak displacements of 1 and 2 mm and peak forces proportional to 33%, 66%, or 100% of the cat’s bodyweight were used. The three forces induced L6 displacements of 1.2 (± 0.2), 2.0 (± 0.5), and 3.3 (± 1.1) mm, respectively. These displacements are comparable to the translation and rotational displacements (1.5 ± 0.5 mm and 20-3.50, respectively) occurring in human cadaveric lumbar spine when high velocity low amplitude thrusts are performed (Ianuzzi & Khalsa, 2005a).
Muscle spindle afferent responses
Activity of individual sensory neurons with a spontaneous resting discharge (15-98 impulses/s) have been studied during the application of spinal manipulative-like loads. (Pickar & Wheeler, 2001; Pickar & Kang, 2006; Pickar et al, 2007). Recordings were obtained from the L6 dorsal rootlets. Afferents were identified as arising from muscle spindles located in lumbar multifidus or longissimus muscles on the basis of their receptive field’s location, their responses to intra-arterial infusion of succinylcholine and/or to electrically-induced muscle twitch. The spindle afferents were further characterized as primary (group 1a) or secondary (group II) based upon their responses to ramp and hold movement of the L6 vertebra. These studies have shown that the spinal manipulation’s thrust phase significantly increases the discharge rate of muscle spindles in the deep lumbar paraspinal muscles (201% ± 57%) compared to the pre-load phase (29% ± 20%) (see Fig 2A) (Pickar & Wheeler, 2001). Recovery of the spindle’s firing rate following the resolution phase may be immediate or take some time (range 100ms - 21.2 s). Furthermore, changing the direction of the applied thrust changes the magnitude of the response.
Lumbar paraspinal muscle spindle response to
a high velocity, low amplitude spinal manipulative-like load.
Many afferents from muscle spindles in the lumbar region demonstrate a graded increase in mean instantaneous frequency when tested across a range of thrust phase durations from 12.5 to 400 ms (see Fig 2B) (Pickar & Kang 2006). In general, group Ia afferents appear more responsive to the spinal manipulative thrust than the group II spindle afferents. Some afferents exhibit an increase only at specific thrust durations. Discharge rate increases by 110-520 impulses/s during a 100ms thrust duration whereas it only increases between 28-88Hz impulses/s during a 800 ms thrust duration (Pickar & Kang 2006). The graded increase in spindle discharge as thrust duration shortens (i.e., as the manipulation’s speed becomes faster) is non-linear, with an inflection occurring at thrust durations less than 150ms. This duration represents one that practitioners often achieve when applying a spinal manipulation clinically to either the lumbar or cervical region (see section above, PHYSICAL CHARACTERISTICS OF SMT). The spindle’s silent period following the resolution phase, which primarily occurs in group Ia afferents, becomes shorter as the duration of the impulse load becomes shorter. Group II spindle afferents do not become silent but it should be noted that their firing interval (inverse of the firing rate) is greater than the silent period of the Group Ia afferents.
Afferent activity in cervical spinal nerves (dorsal rootlets) has been characterised as arising from neck muscle spindles on the basis of it being spontaneous, its receptive field location being confined to a single neck muscle, and an increase in its firing rate in response to an intra-arterial infusion of succinylcholine. However, in contrast to afferents innervating tissues of the low back, afferents innervating the neck are too short in the cat to allow accurate classification as Group I, II, III or IV on the basis of conduction velocity. Nevertheless, it has been possible to study putative muscle spindle activity in the cervical spine. As can be seen in Figure 3, displacement of the C2 vertebra can induce a decrease (Fig 3A) or increase (Fig 3B) in the spontaneous firing of a neck muscle spindle afferents depending on the direction of the displacement. Figure 3 also shows that C2 displacement can induce either an initial pause and then an increase (Fig 3C) or an initial increase followed by a decrease (Fig 3D) in spontaneous discharge. In each case, the spindle’s spontaneous firing rate rapidly returns to the level of the pre-manipulative-like vertebral displacement.
Cervical muscle spindle afferent response to
rapid rotation of the C2 vertebra simulating the thrust
phase of a high velocity, low amplitude spinal manipulation.
Golgi Tendon Organ afferent responses
Afferents with receptive fields in lumbar paravertebral tissues of the cat were deemed to arise from Golgi Tendon Organs (GTO) if 1) they did not exhibit spontaneous activity, but 2) responded to loads with short-lasting, low-frequency activity, 3) had irregular discharge rates in response to an intra-arterial injection of succinylcholine and, 4) had conduction velocities in the group I range (Pickar & Wheeler, 2001). These afferents exhibited responses to SMT-like loading quite different from that of muscle spindles. In particular, GTO afferents were rarely activated by the pre-load phase (with increases in firing rate by >10Hz occurring on only 3 of 15 occasions) and were mildly activated by the thrust phase, increasing their firing frequency by only 21± 4 impulses/s during the thrust phase relative to the control and by only 19 ± 4 impulses/s relative to the pre-load phase. Also in contrast to muscle spindle afferents, GTOs responded even when the direction of the SMT was changed (cranial, caudal or 450 to the spine’s long axis). With few exceptions GTO afferents became silent immediately following the thrust phase and they remained silent. In a second study using a manipulative-like load of 33% body weight (Sung et al 2005), one putative GTO afferent showed a pattern of behavior similar to the muscle spindle afferents when tested over a range of thrust durations but its mean instantaneous firing rate during the thrust phase was substantially less than that of spindle afferents.
Putative Pacinian corpuscles afferents
Pickar & Wheeler (2001) reported the response of one afferent that was inactive at rest and rapidly adapted when the lumbar paraspinal tissues were probed . It responded to an SMT-like thrust (duration: 200ms; peak force: 6.4N) that distracted the facet joint, but it did not respond at loading rates ~10 times slower than the thrust rate nor with peak loads that were up to 4 times higher than the peak thrust force. If this afferent belonged to a GTO it would likely have been activated by the increasing load (Stuart et al, 1970). Because it responded to rate of mechanical loading, it was likely a Pacinican corpuscle (Sato, 1961).
Afferents from the cervical paravertebal tissues are difficult to accurately characterize because they cannot be identified on the basis of their conduction velocity and their receptive fields are difficult to isolate due to the extensive coupled movements of the cervical vertebra when mechanical forces are applied to determine mechanical thresholds. For example, Bolton and Holland (1996) have noted that an afferent responding to a large mechanical force may not in fact represent a high threshold mechanoreceptor such as a GTO located at the site of the applied force, but represent a low threshold mechanoreceptor lying distantly and responding to the dampened mechanical force. It has also been difficult to classify afferents that respond to movement of the C2 vertebra but do not have spontanenous activity and do not respond to intra-arterial injection of succinylcholine (Bolton & Holland, 1996). In this study, some (2/8) afferents had receptive fields in the ipsilateral semispinalis cervicis or semispinalis dorsalis muscles and were activated during movements of the C2 vertebra that lengthened these muscles but not when they were shortened. The responses were rapidly adapting, showing a burst of 3-5 spikes, suggesting they were afferents from either Golgi Tendon Organs or paciniform corpuscles. However, this could not be confirmed. Interestingly, seventy-five percent of the afferents (6/8) were only activated by firm (noxious) pinching of the ipsilateral C2-3 zygapophyseal joint capsule with half (3/6) demonstrating an after-discharge suggesting they conveyed nociceptive information.
It is clear from these studies in the lumbar and cervical regions that impulse loads with force time profiles similar to that of manually delivered high velocity low amplitude thrusts evoke a relatively high-frequency discharge from afferents innervating muscle spindles, GTO’s and high threshold mechanoreceptors. There are currently no unequivocal data regarding whether SMT activates nociceptors.
NEUROPHYSIOLOGICAL CONSEQUENCES OF SMT
THAT MAY UNDERLIE THE EFFECTS OF SMT
The biomechanical findings reviewed above indicate that the nature of the SMT thrust is a dynamic mechanical event. During the manipulation, tissue displacements and forces clearly change rapidly, with no static component, and last only a short time-interval. How could this dynamic, very short-lasting (<150ms) mechanical stimulus change the behaviour of the nervous system in a way that outlasts the intervention itself? The neurophysiological findings reviewed above provide an opportunity to consider a contributory mechanism. It has been suggested that a manipulation’s long-lasting influence on the nervous system can be regarded as a primary and/or secondary event (for example, Pickar, 2002; Leach, 2004; Henderson, 2005; Bialsoky, 2009a). By primary we refer to any long-lasting neural response that arises as a direct consequence of short-lasting neural activity occurring during the manipulation. By secondary we refer to a long-lasting neural response arising as a consequence of (i.e., secondary to) a long-lasting change in spinal biomechanics caused by the manipulation.
A number of sustained changes in spinal biomechanics have been hypothesized to occur as a result of SMT. For example, the impulsive thrust may alter segmental biomechanics by releasing trapped meniscoids, releasing adhesions, or by diminishing distortion in the intervertebral disc (Farfan, 1980; Giles 1989; Lewit, 1991; Haldeman, 1978; Vernon, 1997). Also, individual motion segments are thought capable of buckling thereby producing relatively large vertebral motions that achieve a new position of stable equilibrium (Wilder et al., 1988). The manipulative impulse may provide sufficient energy to restore a buckled segment to a lower energy level thus reducing mechanical stress or strain on soft and hard spinal tissues (Triano, 2001).
Neural responses arising secondary to the long-lasting biomechanical changes may be broadly conceptualized as resulting from neurophysiological changes occurring at either the receptive endings of primary afferents and/or along transmission pathways from these receptive endings. Mechanically-sensitive primary afferents with receptive endings embedded in deep paraspinal tissues respond to mechanical stresses and strains in their local environment (Ianuzzi & Khalsa, 2005a). Long-lasting changes in their mechanical environment could modify the mechanosensory information received by the spinal cord and brain. Signals from chemoreceptors may also be altered to the extent that inflammatory conditions are altered by the manipulation (e.g. see Song et al, 2006). Transmission pathways on the other hand include both peripheral nerves and ganglia where they pass through or lie in the intervertebral foramen, and the spinal cord and brainstem where the latter extends through the foramen magnum into the neural canal. Sustained compressive force on neural tissue at these sites can affect both impulse-based activity (action potential frequency) and non-impulse-based activity (axoplasmic transport) (see Korr, 1978). It has been hypothesized that spinal manipulation can relieve mechanical compression on these transmission pathways and induce beneficial changes in the chemical milieu of these neurons (see Leach, 2004; Henderson, 2005 for a more thorough discussion of this topic).
Activation of Somatosensory Receptors
In 1987, Gillette (Gillette, 1987) proposed that spinal manipulation activates all known mechanosensitive, somatosensory receptors because they all possess mechanical thresholds lower than the peak force delivered during a manipulation and because the 40 in toto receptor-types are responsive to dynamic and/or static components of a mechanical stimulus. The rationale was based upon the one load-time profile for a spinal manipulation that had been recorded at that time (see Gillette, 1987). More recent biomechanical data (see section above, PHYSICAL CHARACTERISTICS OF SMT) indicate a revision to this load-time profile is needed. A high-velocity, low amplitude spinal manipulation, which over 90% of chiropractic patients receive as part of their care (Christensen, 2005), is purely dynamic, with a short rise-time to its peak amplitude, and with no static component (see Figure 1). Based upon these features, the proposed receptor population responsive to a spinal manipulation can be reduced by more than half, to only those that have a substantial dynamic component. Thresholds of these afferents are less than 20-30N (see Table 2 of Gillette, 1987), and represent magnitudes less than a manipulation’s peak force. Thus, all four classes of primary afferents neurons, [Group Ia, Ib, and II (Aβ), III (Aδ) IV (C) fibers] would be expected to respond during the manipulation. However, vertebral tissues could act as low-pass mechanical filters, reducing the stimulus’s dynamic component. In the extreme, the applied load may dissipate and it’s magnitude become insufficient to activate these sensory receptors. Nevertheless, recordings of multi-unit and single-unit activity in paraspinal primary afferents show that spinal manipulation does indeed stimulate paraspinal afferents (see section above, STUDIES OF PARAVERTEBRAL SOMATOSENSORY AFFERENT ACTIVATION DURING SMT-LIKE MOTION).
To date, only muscle spindle afferents in the low back have been systematically studied and their response to spinal manipulation characterized (see section above, Muscle spindle afferent responses). Their non-linear behaviour in response to the duration of the manipulation’s thrust phase might not be considered surprising based upon the long-known velocity sensitivity of spindles studied in limb muscles. Like limb muscle spindle afferents (e.g. see Figure 10 in Matthews 1963), paravertebral Group Ia spindle endings show a response inflection. This inflection represents a threshold for higher spindle discharge frequencies than would otherwise be predicted from their discharge frequencies evoked by slower stretch rates. Most interestingly, this threshold stretch rate (~10mm/s) is comparable to the rate at which a spinal manipulation imparts movement to a vertebra, translating it less than 3 mm in less than 150 ms (see above Vertebral Motion with SMT).
Muscle spindles also demonstrate another type of dynamic threshold when their sensitivity has been studied using sinusoidal stretch-shortening cycles. In the limbs, both Group Ia and Group II muscle spindle afferents show a non-linear increase in sensitivity at sinusoidal loading rates of 1.5 cycles/s (e.g. see Figure 5 in Matthews & Stein 1969). It can be seen in Figure 2B that when a spinal manipulation is modelled as a half-sine wave the manipulative thrust represents one-quarter cycle. A thrust duration of 150ms would represent a loading rate of 6.7 cycles/s and would be faster than the sinusoidal rate threshold for augmented spindle sensitivity. Together, these findings suggest that one consequence of a spinal manipulation is that it creates a higher frequency sensory input from muscle spindles than otherwise occurs during daily spinal motion. The sensory barrage from the population would be relatively synchronous in time, occurring over the time interval of the thrust (< 150ms) and vertebral motion that accompanies it. The sensory inputs would likely arrive at the central nervous system from a relatively localized area of the spine (see above, Vertebral Motion with SMT).
By comparison with muscle spindles, the relationship between the velocity of an applied mechanical stimulus and the discharge pattern of mechanosensitve, non-spindle afferents in either the vertebral column or the limbs is virtually unknown. For example in the finger, Edin et al. (1995) showed that discharge rates of dynamically-sensitive, cutaneous Group II mechanoreceptors increased as the velocity of skin indentation increased. The formal relationship between the two was not characterized. Similarly, A-δ and C-fiber mechanonociceptors are known to fire an initial high burst during a dynamic mechanical stimulus application (Mense, 1986; White & Levine, 1991) but how the duration of the their discharge frequency is formally related to either the magnitude or velocity of the stimulus is not known. If paraspinal non-spindle afferents are also activated by a spinal manipulation (see above, Other Afferents), it seems reasonable to think that they too present a burst of high frequency activity to the central nervous in a synchronous manner and from a localized area of the spine.
Knowledge that SMT-like movements produce a short-lasting, high frequency barrage of action potentials (see above) raises the possibility that SMT may induce longer term effects by modulating the central nervous system. Nearly 3 decades ago studies showed that synaptic efficacy is affected by the history of high frequency bursting from group Ia and group II muscle afferents(Davis et al, 1985, Luscher et al., 1983; Collins et al., 1984). The effect lasted beyond the duration of the burst itself. In α-motoneurons, bursts of action potentials with short interspike intervals affected the magnitude of post-synaptic potentials differently from longer interspike intervals. In addition, α-motoneurons are bi-stable and can sustain plateau potentials. Brief periods of excitation can switch them into a period of self-sustained firing (Hounsgaard et al, 1986). Such a state appears to have consequences for the normal production of muscle force (Collins et al, 2002). Such processes may underlie experimental findings showing changes in parameters related to increased muscle excitability following SMT (Suter et al, 2000; Dishman et al, 2002; Keller and Colloca, 2000; Koppenahaven et al, 2011).
High frequency stimulation of small diameter A-δ and C-fibers also affects synaptic efficacy. Both long-term potentiation as well as depression have been produced (Randic et al., 1993). The change in behaviour of second order neurons lasts up to 1 hour following the initial sensory barrage (Randic et al., 1993,Ikeda et al, 2000). In these experiments, a peripheral nerve was electrically stimulated thereby synchronously activating the afferent population. The whole nerve was stimulated at 100 Hz over a short lasting interval (~1s) and was given several times at ~10s intervals. The physiological relevance of such a stimulus has been questioned because C- and perhaps A-δ fibers do not typically discharge at such high rates, but stimulation using more intermediate frequencies (20Hz) also produces long-lasting changes (3-6 hours) in synaptic efficacy (Liu & Sandkühler, 1997). The stimulus durations are clearly longer than a manipulative stimulus (< 150ms) however, we currently lack knowledge regarding how short a duration is capable of eliciting a change in synaptic efficacy. In addition, it is not know what discharge rates are evoked in paraspinal C- and A-δ fibers by spinal manipulation. While changes in synaptic efficacy produced by high frequency stimulation paradigms have been applied toward understanding cellular mechanisms underlying hyperalgesia (Sandkuhler, 2009), they also provide a reasonable basis for considering how the short-lasting, dynamic mechanical input of a spinal manipulation produces a neural response that outlasts the intervention itself. This neurophysiological process may underlie findings from clinically-oriented basic science studies showing that spinal manipulation reduces temporal summation of thermal stimuli delivered to the periphery (George et al, 2006; Bialosky et al, 2009b; Bishop et al. 2011).
In conclusion, spinal manipulation could affect the nervous system by activating paraspinal sensory neurons during the maneuver itself and/or by altering spinal biomechanics. Biomechanical changes which follow the manipulation would, in turn, modulate paravertebral sensory neuron signals. As a short-lasting, dynamic mechanical stimulus, spinal manipulation may take advantage of two signalling characteristics of the nervous system: 1) inherent high frequency signalling properties of dynamically-sensitive primary afferent neurons and 2) response properties of post-synaptic neurons. Experimental studies reveal that spinal manipulation evokes a high frequency discharge in some primary afferents. In experimental studies not using spinal manipulation, spatial and/or temporal summation of high frequency input produces sustained changes in synaptic efficacy. Future studies directed at understanding how central neurons are affected by high frequency sensory input from paraspinal tissues during the manipulation are warranted based upon the literature and should contribute to our understanding of the mechanisms for spinal manipulation’s action.
JG Pickar’s research is supported by grants from the National Center for Complementary and Alternative Medicine (NCCAM). Some investigations were conducted in a facility constructed with support from Research Facilities Improvement Grant Number C06 RR15433 from the National Center for Research Resources, National Institute of Health.
PS Bolton’s research is supported by grants from the National Health and Medical Research Council of Australia and the Australian Spinal Research Foundation.
Joel G. Pickar, is a Professor at the Palmer Center for Chiropractic Research at the Palmer College of Chiropractic in Davenport, IA. He earned his Doctor of Chiropractic from Palmer College of Chiropractic in 1977 and his PhD in physiology from University of California Davis in 1990.His research laboratory studies neurophysiological issues related to the vertebral column and to chiropractic manipulation.
Philip S. Bolton, was awarded a BSc (Physiology) from the University of New England (Australia) in 1976, his Doctor of Chiropractic (DC) from Palmer College of Chiropractic (USA) in 1980 and his PhD in Neuroscience from University of New South Wales (Australia) in 1990. He completed postdoctoral training at the Rockefeller University (USA), and has been a visiting scientist at the University of Pittsburgh (USA), the Prince of Wales Medical Research Institute (Australia) and the University of Sydney (Australia). He is a senior investigator in the Pain and Sensory Dysfunction Research Group at the University of Newcastle’s Priority Research Centre for Translational Neuroscience and Mental Health.
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