A lack of variability in people with pain? I’m intrigued…

A recent paper by Falla and colleagues [1] evaluated back muscle activity (via electromyography) during a repetitive lifting task and compared two groups: a chronic/recurrent low back pain group and a healthy control group. What is unique about this study is that they evaluated back muscle activity using a grid of electrodes to characterise the distribution of activity over a large portion of the erector spinae musculature. Based on the finding that people with experimentally-induced back pain exhibit increased variability in the pattern of trunk muscle activation during slow trunk flexion/extension movements (compared with no pain)[2] it is tempting to predict that by measuring more sites within an area, we might just see more variability.

It is fascinating, then, to consider the authors’ findings that during performance of the lifting task there was not increased variability in the distribution of muscle activity in people with back pain, but rather, decreased variability over time compared with healthy controls. While tempting to speculate that this reduced variability might be a result of group averaging, post-hoc comparisons of individual participant data generally support the findings.

And these were the findings: in healthy controls, the main location of back muscle activity shifted in a caudal direction over time. That is, during repetitive lifting, the EMG root mean square (a measure of the amplitude or magnitude of muscle activity) progressively increased over time in the caudal region of the lumbar spine erector spinae musculature. Additionally, the EMG centroid (a value [x,y coordinates] that is calculated by considering muscle activity from all electrodes and thus provides a location that is representative of overall muscle activity) also shifted caudally over time. Together these findings demonstrate a shift in the distribution of muscle activity during repetitive lifting. However, in people with back pain, while EMG amplitude increased over time (suggesting increased activity in the same region of the back muscles over time), the distribution of muscle activity remained the same. The authors suggest that these findings might show a maladaptive response (ie, lack of variability) in people with low back pain when performing repetitive tasks.

The paper does an excellent job of discussing the peripheral mechanisms that may account for these changes (or lack of changes) in muscle activity in people with back pain. Now I am not for one minute disputing that peripheral factors influence muscle activity – of course they do and the existence of entire fields of research to study these properties pay testament to that. However, I am suggesting that what we know about motor cortical neuroplasticity would be relevant to consider in interpreting these findings.

First, there is evidence to suggest that pain alters the excitability of the motor cortex. For example, functional magnetic resonance imaging studies have found a transient increase, followed by a prolonged reduction of contralateral motor cortex signal intensity during pain induced by injection of the masseter muscle with hypertonic saline but not when the muscle is injected with isotonic saline.[3]

Second, this reduction in motor cortex excitability with the presence of pain appears to block motor learning. For example, after undergoing a novel tongue-protrusion training task, motor cortex excitability is increased (as evaluated by measuring the motor evoked potentials in the tongue musculature induced by transcranial magnetic stimulation of the motor cortex).[4] However, when capsaicin is applied to the tongue and then the training occurs, there is no change in motor cortex excitability and task performance is impaired.[4] That is, the neuroplasticity of M1 appears blocked by the presence of pain.

Now the relationship between ongoing pain and motor cortex excitability is complex[5], but what the general findings suggest is that the inherent capability to learn new motor patterns or strategies may be reduced in people with pain. Thus in situations where peripheral muscular fatigue occurs, the lack of variability in cortical activation patterns may be incredibly important.

I commend the authors on a very interesting and well-written study and merely wonder in the background, is reduced variability in distribution of muscle activation suggestive of being ‘stuck in a motor groove’ cortically and if so, how might we best target this in treatment?

Tasha Stanton

grey A lack of variability in people with pain? I’m intrigued…

Tasha Stanton is a postdoctoral research fellow working with the Body in Mind Research Group in Adelaide at University of South Australia as well as in Sydney (at Neuroscience Research Australia). Tash has done a bit of hopping around in her career, from studying physio in her undergrad, to spinal biomechanics in her Master’s, to clinical epidemiology in her PhD, and now to clinical neuroscience in her postdocs. Amazingly, there has been a common thread through all this hopping and that common thread is pain. What is pain? Why do we have it? And why doesn’t it go away?

Tasha got herself one of the very competitive NHMRC early career fellowships and is well on the way to establishing her own line of very interesting investigations.  Her research interests lie in understanding the neuroscience behind pain and its clinical implications. She also really likes nifty experiments that may have no clinical value yet, but whose coolness factor tops the charts. Last, Tash is a bit mad about running, enjoying a good red with friends and organizing theme parties. Tasha, aka Stanton Deliver, was the all round best performer at the Inaugural BiM Table Tennis Comp. Here is Tasha talking more about what she does and a link to her published research.

References

[1] Falla D, Gizzi L, Tschapek M, Erlenwein J, & Petzke F (2014). Reduced task-induced variations in the distribution of activity across back muscle regions in individuals with low back pain. Pain, 155 (5), 944-53 PMID: 24502841

[2] Hodges PW, Coppieters MW, MacDonald D, & Cholewicki J (2013). New insight into motor adaptation to pain revealed by a combination of modelling and empirical approaches. Eur J Pain, 17 (8), 1138-46 PMID: 23349066

[3] Nash PG, Macefield VG, Klineberg IJ, Gustin SM, Murray GM, & Henderson LA (2010). Changes in human primary motor cortex activity during acute cutaneous and muscle orofacial pain. Journal of orofacial pain, 24 (4), 379-90 PMID: 21197510

[4] Boudreau S, Romaniello A, Wang K, Svensson P, Sessle BJ, & Arendt-Nielsen L (2007). The effects of intra-oral pain on motor cortex neuroplasticity associated with short-term novel tongue-protrusion training in humans. Pain, 132 (1-2), 169-78 PMID: 17870237

[5] Di Pietro F, McAuley JH, Parkitny L, Lotze M, Wand BM, Moseley GL, & Stanton TR (2013). Primary motor cortex function in complex regional pain syndrome: a systematic review and meta-analysis. J Pain, 14 (11), 1270-88 PMID: 24035350

Comments

  1. Hi Tasha
    Thanks for a great summary. Your comments on the role of the brain/cortex in these findings are hard to dispute.
    Another thought i had on reading the paper was whether experimentally-induced pain can still be thought of as a useful surrogate for chronic, long-lasting disabling pain (as opposed to acute or short duration pain) – specifically in terms of the context/meaning of the 2 different types of pain (experimental/no fear versus chronic disabling/fear/impact on life etc..). any thoughts on whether this might explain the differences in variability between these 2 study designs?

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  2. John Quintner says:

    Tasha, I agree that this is a fascinating and important study.

    First, I must challenge two of your statements: (i) “pain alters excitability of the motor cortex”; (ii) “neuroplasticity appears to be blocked by the presence of pain”. As I have pointed out before, “pain” cannot be both a lived experience and an agent of physiological change.

    However, the suggestion that there may be a lack of variability in cortical activation in patients with low back pain reminded my of an old paper by Walter J Freeman. [The physiology of perception. Scientific American 1991; 264: 78-85]

    “Our studies have led us as well to the discovery in the brain of chaos- complex behavior that seems random but actually has some hidden order. The chaos is evident in the tendency of vast collections of neurons to shift abruptly and simultaneously from one complex activity pattern to another in response to the smallest of inputs. This changeability is a prime characteristic of many chaotic systems. It is not harmful in the brain. In fact, we propose it is the very property that makes perception possible. We also speculate that chaos underlies the ability of the brain to respond flexibly to the outside world
    another in response to the smallest of inputs and to generate novel activity patterns.”

    Is it possible that the data from this study can be explained on the basis that the the patients with spinal pain were exhibiting a loss of this fundamental neurophysiological property in relation to their ability to generate novel activity patterns within their spinal musculature?

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  3. John Quintner says:

    Please delete “another” from the second last line of the quote from Walter Freeman. Sorry!

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  4. Thankyou for this post – really interesting

    Two possible (and overlapping) mechanisms that come to mind are

    a) there is a reduced adaptive capacity due to other internal loads on the musculoskeletal system

    b) the pain is in muscles that CAN work, because they are already being over-used

    There is another interesting paper – on mirror neuron inhibition – http://rstb.royalsocietypublishing.org/content/369/1644/20130174.full.pdf which may have some bearing on this

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  5. stuart miller says:

    Andrew, I am curious as to how you came up with the idea that ‘the pain is in muscles that CAN work because they are already being over-used’ – I can understand that there would be altered signalling to the cortex. I still like the idea of internal loads on the musculoskeletal system in guiding behaviour that eventually becomes more rigid (less variable) in response to repetition. An interesting paper by Bennett, KM and Lemon, RN underlies the complexity of movement patterns ‘Cortico-motoneuronal contribution to the fractionation of muscle activity during precision grip in the monkey’
    John, could you provide some direction to me in making sense of the chaos (a bit) ? Are there not resting state networks (ex DMN) that are ‘switched off’ by salient input (ex SN) that guide the search for movement patterns via multi-sensory integration at multiple levels ? I’ll re-read Freeman’s paper…

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  6. John Quintner says:

    Stuart, it seemed to me that the researchers were investigating the dynamics of a non-linear system.

    Tasha, do you agree?

    Freeman’s work on olfaction in rabbits utilized a grid on the olfactory bulb and they uncovered some fascinating patterns, as you will read in his article. Another context in which the dynamics of non-linear systems is being studied is that of heart rate variability and its relation to heart disease. There are some interesting studies that can be easily accessed on-line. Loss of heart rate variability seems to be an important marker of the “sick” heart but it also can be observed in the ageing heart.

    Could a similar loss of variability, as demonstrated in this study, be a marker of a “sick” back?

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  7. Hi Stuart

    I use several diagnostic tools, most of which look one way or another for areas of the body that are less mobile than they should be. Most times, pain – especially lower back pain – is not the focus of immobility, but is secondary to less mobility in other areas of the body – which, if treated and made more mobile/functional, often result in the pain disappearing. Visceral adhesions (especially abdominal, and especially where there is a history of surgery) are fairly common factors in LBP.

    The paper you quoted points in a similar direction to the one I suggested – precision grip is managed by the pyramidal tract – which is a major location of inhibitory premotor mirror neuron activity. If its inhibitory function is overactive for some reason, this could result in a loss of motor adaptability (?) It’s a slightly obtuse argument, but it does neatly explain how dissociation might work at the musculoskeletal level.

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  8. stuart miller says:

    Tasha,
    Thanks again for the report. In terms of variability, it makes sense to me that with experimentally induced pain, that there would be increased variability as there is a search for a motor pattern that is helpful in the presence of nociceptive input. Eventually, habitual patterns of movement develop – we are usually trying to shape these patterns as therapists. Early on, if there is inflammation (whether neurogenic or otherwise) there are limitations to the availability of movement patterns (especially into end range) especially under increased load or speed.
    Andrew, I agree with you that if you can restore the luxury of movement patterns (and degrees of freedom) that the CNS is used to, you can allow a search for a more effective pattern.
    John, I re-read the Freeman paper – I like the analogy with the choral piece in which you have to hear the performers together to discern a pattern. I think the integration piece in terms of processing visual and auditory information about external stimuli (secondarily olfactory info) with tactile and proprioceptive information about our body parts allows the search for an appropriate motor plan. At the start and end of a movement pattern (especially with habitual patterns) I thought there was more cortical activity – this might be where there is increased processing re the threat of a movement (OK +, OK -). Thoughts ?

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  9. stuart miller says:

    Tasha, sorry, the first sentence should say ‘that is helpful in the presence of salient nociceptive input.’
    I think it was Bernstein that developed the theory of multi-level hierarchical control of voluntary movement around the degrees of freedom problem – the theory has since been updated. He saw minimal variability in movement patterns with professional blacksmiths in their hitting movements – habitual patterns in experts (not just pyramidal tract – subcortical activity, rubrospinal tract etc. – we augment the underlying motor synergies with cortical control – may also explain some of the chaos with EEG (even quantitative)). It would be cool if they went back and looked at cortical activity throughout habitual movement patterns (rather than with rats in mazes – we split from that group about 80 million years ago).
    I think the hierarchical control lies in the evolution of vertebrates – we have only been upright for ~ 4 million years and only had the brain power for half that time – still working on our upright movement patterns as 80% of those who have experienced back pain will attest. I really like Peter Sullivan’s work with movement patterning. It would be cool if they could slap the electrodes on some of the people he sees after his education sessions and look at the variability and see if there is a resumption of posterior shift in EMG with repetition. Thoughts ?

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  10. stuart miller says:

    Tasha,
    I realize you are busy – other than being stuck in a groove cortically – could you address John’s question about the dynamics of a non-linear system or could you speculate on the underlying reasons for the lack of caudal shift in EMG activity with the chronic/recurrent LBP group and/or why is there a lack of cranial shift in trapezius muscle activity in another study (Falla’s work in 2010)? Thanks for the post – looking for further insight…

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  11. John Quintner says:

    Stuart, trying to understand the dynamics of non-linear systems in relation to the experience of pain is probably far beyond us at the moment but I suspect that by exploring the implications of such system properties we might be able to improve our current concepts of pain management.

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  12. Tasha Stanton says:

    Hi all,

    What a great bunch of posts and interesting discussions! My apologies for the radio silence…I am madly treading water at the moment trying to stay above the to-do list, but my head remains under, so I’m sure you will forgive my delay.

    Kieran, I take your point about experimental pain – you are spot on. I don’t think that we would expect to see identical things with chronic pain, where certainly I would argue that the threat value of different movements is very different to that scenario of experimental pain. There was a study of people with chronic back pain that showed increased variability of their muscle activation (ie, reaction times) compared with healthy controls when performing a task that involved a sudden release of trunk loading. This might be a more relevant example to support the hypothesis of why we might expect more variability in people with pain. However, there is also evidence (article by Jacobs and colleagues in 2009) that shows that people with chronic low back pain have reduced variability in the timing of their anticipatory postural adjustments, suggesting that the story isn’t probably as clear as we’d like!

    Radebold et al. Muscle response pattern to sudden trunk loading in healthy individuals and in patients with chronic low back pain. Biomechanics 2000; 25:947-954.

    Jacobs et al. People with chronic low back pain exhibit decreased variability in the timing of their anticipatory postural adjustments. Behav Neurosci 2009;123:455-458.

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  13. Tasha Stanton says:

    John – regarding the non-linear system stuff…I think this is a very relevant suggestion. It is also one that is getting out of my comfort zone in terms of knowledge! In a purely mathematical sense, (I’m not sure if you meant this John?), it is my understanding that a system is non-linear when a dependent variable (or a derivative of that variable) is raised to a power greater than 1…or in other words, when the response of one variable to a change in another variable cannot be fitted to a straight line. Thus the behaviour of the system (output) is not equal to the sum of the linear variables that are part of the system. I reckon this would definitely seem to be applicable in movement. For example, that the relationship between EMG and torque changes at high levels of muscle activation suggests that the system is non-linear (a peripherally-based example). Further, non-linear systems, like a pendulum, often exhibit predictable behaviour within a certain range, and yet when this range is breached (ie, large swings of the pendulum), they can behave strangely or unpredictably. This sounds very much like the complexities of movement!! I think in experimental tasks of trunk movement, the system is sometimes treated as a linear system so that it can be more easily modelled, but I would assume that it likely isn’t linear. There was an interesting article in BMJ about muscular fatigue being a non-linear process.

    Lambert et al Complex systems model of fatigue: integrative homeostatic control of peripheral physiological systems during exercise in humans. Br J Sports Med 2005;39:52-62.

    I do really like this idea of ‘cortical flexibility’ whereby variability is adaptive. I think you are spot on with the suggestion of a ‘sick-back’ John. It certainly has been a point that has been considered: See Moseley and Hodges’ work in Behavioural Neuroscience 2009; 120:474-476 (reduced variability of postural strategy prevents normalization of motor changes induced by back pain: A risk factor for chronic trouble?).

    I also wonder how much ‘excess cognitive control’ of movements influences this lack of variability in people with pain. For example, when I have something that is sore, I tend to think very carefully about how to move that body part and continuously attend to it and monitor it during movement instead of just naturally moving it. So in people with back pain I wonder how much of the lack of variability was due to an excess of cognitive control over movement patterns, instead of just allowing movement patterns to naturally change. Perhaps this illustrates the importance of ‘unconscious’ movement patterns for lack of a better term. That is, ‘unconscious’ in the sense that you don’t hyper-attend to the movement pattern (ie, where ‘hyper-attending’ involves constantly, consciously controlling and re-evaluating the movement).

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  14. Tasha Stanton says:

    Stuart – great study ideas as always. It would be intriguing to consider movement pattern/muscle activation variability as an outcome measure. However, I think it becomes important to follow longitudinally – was the lack of variability there prior to back pain onset? And if so, is this predisposing? Further, is the lack of variability truly the problem or is it merely a marker of other problems? If we target muscle activation pattern variability in treatments, then do we see improvements in outcomes? All very interesting questions I think…

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  15. John Quintner says:

    Tasha, thanks for your many interesting insights.

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