1

MUSCLE DYSFUNCTION IN CERVICAL PAIN AND THE IMPLICATIONS FOR TRAINING

Deborah Falla

CENTER FOR ANESTHESIOLOGY, EMERGENCY AND INTENSIVE CARE MEDICINE, UNIVERSITY HOSPITAL GÖTTINGEN, GERMANY

DEPARTMENT OF NEUROREHABILITATION ENGINEERINGBERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCEUNIVERSITY MEDICAL CENTER GÖTTINGEN, GERMANY

� Changes in sensorimotor control are an almost obligatory feature of musculoskeletal conditions

� Evidence for modification of motor and/or sensory functions has been reported for a broad array of conditions, and these changes have become common targets for rehabilitation

� It has been assumed that sensorimotor changes are relevant for the development, perpetuation or recurrence of pain and/or injury

� Reflect on these assumptions in relation to neck pain

Models of motor adaptation to pain

Musclepain

Group III & IVexcitation

Increasedmuscle activity

Muscleischemia

Vicious cycle theoryJohansson & Sojka. 1991

Musclepain

Group III & IV excitation

Decreased agonisticmuscle activity

Increased antagonisticmuscle activity

Inhibition ofα-motoneurons

Excitationα-motoneurons

This pathway is facilitated in case of agonistic muscle

activity

This pathway is facilitated in case of antagonistic

muscle activity

Pain adaptation theoryLund. Can J Physiol Pharmacol. 1991

2

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

3

100 200 300mV0

10

20

30

40

•

200

400

600

800

1000

1200

Subtle changes in the distribution of activity -High density surface EMG

LateralMedial

Cranial

Caudal

y-axis

x-axis

No redistribution of upper trapezius muscle activity during sustained contractions in patients with trapezius myalgia

Control

Cranial

Caudalx-axis

y-a

xis

Medial Lateral

0 – 5 s 55 – 60 s

140

120

100

80

60

40

20

0 µV

Trapezius Myalgia

0 – 5 s 55 – 60 s

Falla et al. J Electromyogr Kinesiol. 2009

140

120

100

80

60

40

20

0 µV

acromion

C7

Shift in the distribution of activity across the trapezius muscle with experimental neck pain

Barbero, et al. 2015

BaselineIsotonicHypertonicRecovery

10 20 30 40 50 60 70 80 90 10095

100

105

110

115

120

125

130

Percentage of Cycle (%)

Y-a

xis

ce

ntr

oid

(%

)

*

*

**

*

**

*

*

Caudal

Cranial

*

4

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

Persistence of the motor adaptation could also underpin reduced

“confidence” in the injured /painful region, thus promoting disuse or

modified use of the body part, that is, the adapted motor behaviour could

interact with psychosocial issues

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

5

0

0.2

0.4

0.6

0.8

1

1.2

1.4

1.6

1.8

EMG

am

plit

ud

e n

orm

alis

ed

to b

ase

line

S1 S2 S3 S4 S5 S6 S7 S8

RHYO

RSTER

RSCA

RUTR

RLTRLHYO

LSTER

LSCA

LSPLLUTR

LLTR

Gizzi et al. 2015

Individual changes in response to experimentally induced neck muscle pain

Decreased Unchanged Increased

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

Despite the diversity of adaptation in muscle activation in pain, the net effect

of the adaptation appears to have the general aim to protect the

painful/threatened body part from real or anticipated further

pain or injury

6

60

240

30

210

0

180

330

150

300

120

270 90

60

240

30

210

0

180

330

150

300

120

270 90

Left Sternocleidomastoid Right Sternocleidomastoid

Left Splenius Capitis Right Splenius Capitis

60

240

30

210

0

180

330

150

300

120

270 90

60

240

30

210

0

180

330

150

300

120

270 90

°

°

°

°

mean resultant vector (preferred direction)

Falla et al. Clin Neurophysiol. 2010

EMG Tuning Curves

Left Sternocleidomastoid Right Sternocleidomastoid

Left Splenius Capitis Right Splenius Capitis

60

240

30

210180

330

150

300

120

270 90

60

240

30

210180

330

150

300

120

270 90

0 0° °

60

240

30

210180

330

150

300

120

270 90

60

240

30

210180

330

150

300

120

270 90

0 0° °

mean resultant vector (preferred direction)

Falla et al. Clin Neurophysiol. 2010

EMG Tuning Curves

60

240

30

210

0

180

330

150

300

120

270 90

°

Directional specificity of muscle activity is reduced in persons with neck pain

15 N contraction , 0-360°

Relative muscle specificity to direction

Neck PainControls

Left SCM

Right SCM

Left SCap

Right SCap

Falla et al. Clin Neurophysiol. 2010

7

Average amplitude of neck muscle activity is increased

0

10

20

30

40

50

60

70

80

Right SCM Left SCM Right SCap Left SCap

Neck PainControls

EMG

am

plit

ud

e (

µV

)

Falla et al. Clin Neurophysiol. 2010

*

*

**

Assessment of trunk rotations during gait with and without the head turned

Falla et al. 2015

Pelvis

0 10 20 30 40 50 60 70 80 90 100-10

0

10

% gait cycle

Ang

le (

°)

Thorax-Pelvis

-10

0

10Thorax

-10

0

10

Neck Pain

Controls

Hip

ra

ng

e

of

mo

tion

(°)

Kn

ee

ra

ng

e

of

mo

tion

(°)

An

kle

ran

ge

o

f m

otio

n (

°)

3 km/h Self-selected 5 km/h

Neutral (L) Rot (R) Rot Neutral (L) Rot (R) Rot Neutral (L) Rot (R) Rot

L R L R L R L R L R L R L R L R L R Falla et al. 2015

Hip

Kn

ee

An

kle

8

0

2

4

6

8

10

12

14

16

18

0

2

4

6

8

10

12

14

16

18

0

2

4

6

8

10

12

14

16

18

Tru

nk

rota

tio

n (

°)

Neutral (L) Rot (R) Rot Neutral (L) Rot (R) Rot Neutral (L) Rot (R) Rot

3 km/h Self-selected 5 km/h

Neck PainControls

Falla et al. 2015

Reduced trunk rotations in neck pain during gait with the head turned

* *

* *

* *

Reduced trunk rotations in neck pain during gait with the head turned

Diff

ere

nc

e t

run

k ro

tati

on

: N

eu

tra

l-he

ad

ro

tati

on

(°)

Neck Pain

Controls

3 km/h Self-selected 5 km/h

L R L R L R

-3.5

-3

-2.5

-2

-1.5

-1

-0.5

0

* * * * * *

Falla et al. 2015

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2015

9

Trapezius Myalgia

0 – 5 s 55 – 60 s

140

120

100

80

60

40

20

0 µV

Control - Baseline Acute Experimental Pain

Cranial

Caudalx-axis

y-a

xis

Medial Lateral

0 – 5 s 55 – 60 s 0 – 5 s 55 – 60 s

Experimental muscle pain inhibits the

redistribution of muscle activity during sustained contractions

Falla et al. J Electromyogr Kinesiol 2009

Falla et al. Clin Neurophysiol. 2009

No PainPain

0

2

4

6

8

10

12

T2 s

hif

ts (

ms)

-2C0-1

Longus Capitis

C2-3 C0-1

Longus Colli

C2-3

**

**

0

1

2

3

4

5

T2 s

hif

ts (

ms)

Right

SCM C2-3

Left Right

SCM C6-7

Left

*

Cagnie et al., Man Ther, 2011

Experimental muscle pain induces the same change in neck flexor muscle coordination

Control

Neck pain

0

20

40

60

80

100

120

140

Stage of C-CFT (mmHg)

DC

F n

orm

alis

ed

RM

S v

alu

es

(%)

0

30

60

90

120

150

180

22 24 26 28 30

SCM

no

rma

lise

d R

MS

va

lue

s (%

)

*

*

*

**

*

*

Falla et al. Spine; 2004

Sensorimotor deficits could contribute to the development of injury/pain if, for example;

(i) the strategy of movement/muscle activation involves components that load the tissues excessively

(ii) inaccurate sensory information about the movement leading to inaccurate control

(iii) the movement involves too much or too little variability

Reorganization of muscle activity may lead to

pain or perpetuate pain

10

� In people with neck pain but no back pain -those with poor ability to perform a voluntary activation of the lower abdominal muscles, were 3–6 times more likely to develop persistent or recurrent LBP in the following two years than those who performed well on this task Moseley 2004

� Development of pain may be mediated by suboptimal tissue loading related to the “new” movement pattern adopted after the initial exposure to nociceptive input/pain e.g. development of back pain secondary to modified gait in low limb injury Nadler et al., 2000

Reduced motor control may lead to pain

Contemporary theory proposes that the motor adaptation:

(i) involves a diversity of changes from subtle changes in the distribution of activity within and between muscles

to complete/relative avoidance of movement;

(ii) is specific to the individual;

(iii) has a general aim (at least in the short term) to protect the painful/threatened body part from real or

anticipated further pain/injury;

(iv) may precede or follow the onset of pain/injury;

(v) has potential long term consequences if it is maintained, excessive or inappropriate

Hodges and Falla. GMMPT. 2014

Boudreau & Falla, Exp Brain Res 2014

Onset of neck muscle activation in response to full body perturbations

0 100 200 300 400 500

Time (ms)

Control

R SCM

L SCM

R SCap

L SCap

600

Neck Pain

0 100 200 300 400 500

Time (ms)

600

Forward Slide 10˚ Backward Tilt10˚ Forward TiltBackward Slide

11

Forward Slide 10˚ Backward Tilt10˚ Forward TiltBackward Slide

Boudreau & Falla. Exp Brain Res. 2014

Onset (ms)

Delayed neck muscle activity in response to full body perturbations

ControlsNeck pain

50 70 90 110

FT

FS

BS

BT

50 70 90 110

FT

FS

BS

BT

Onset (ms)

Sternocleidomastoid Splenius Capitis

*

*

*

*

*

*

*

*

Elliott et al., PLoS ONE, 2011

Control

Whiplash patients with moderate to severe pain

Increased muscle fatty infiltrate

in patients with severe pain by 3

months after onset of pain/injury

0

0.1

0.2

0.3

0.4

1 3Time Post Injury (Months)

Tota

l MFI

Fatty infiltration of muscle tissue occurs soon following neck trauma but not immediately

*

Changed motor output/

mechanical behavior:Change - stiffness, force direction,

load distribution, variability, force & movement amplitude

Long term consequences:Increase potential for injury &/or nociceptor provocation injured tissues & other body segments -�load, invariable load, �shock

absorption, deconditioning

Load exceeds tissue tolerance

Discrete excessive loadAccumulated load

(Posture, function, etc.)

Short term benefit:Protection of the injured/painful region – �muscle activity/stress, �movement, �potential for error

Psychosocial features

Fear/attitudes/beliefs

Mismatch between motor

output - sensory input

Subtle Redistributed activity within & between muscles

Sensitized nervous system

Mechanism:

changes in

sensorimotor system

Motor cortex excitability/

organisation, sensory cortex, cognitive-

emotional,sensory integration,

sensorimotor mismatch,brain stem, spinal

cord (e.g. inhibition/excitation), receptor injury

etc)

MajorAvoidance of

movement

Changes in motor behavior

Real or threatened

nociceptive input/pain/injury

Hodges and Falla. GMMPT. 2015

12

Is training effective for restoration of motor function?

Design of Study

� Patients with chronic neck pain

� Randomized into 1 of 2 groupsmotor relearning program of specific exercise control: act as usual

� 8 week exercise intervention

� Measures baseline and week 9

� Outcome assessment: Directional specificity of neck muscle activity

Falla, et al. Eur J Pain. 2013

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

Pre Post

Pre Post

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

60

240

30

210

0°

180

330

150

300

120

270 90

Tra

inin

g

Ac

t a

s u

sua

l

(R) SCM(L) SCM

(R) SCap(L) SCap

(R) SCM(L) SCM

(R) SCap(L) SCap

(R) SCM(L) SCM

(R) SCap(L) SCap

(R) SCM(L) SCM

(R) SCap(L) SCap

60

240

30

210

0°

180

330

150

300

120

270 90

Falla, et al. Eur J Pain. 2013

13

Training

15 N contraction , 0-360°Relative muscle specificity to direction, RSD (%)

Act as usual

15 N contraction , 0-360°Relative muscle specificity to direction, RSD (%)

60

240

30

210

0

180

330

150

300

120

270 90

°

60

240

30

210

0

180

330

150

300

120

270 90

°

PrePost

Left SCM

Right SCM

Left SCap

Right SCap Falla, et al. Eur J Pain. 2013

Enhanced directional specificity of muscle activity following training

Is training effective for relief of pain?

Symptomatic relief following motor control training in neck pain

Falla et al. Clin Neurophysiol. 2006

MILD IDIOPATHIC

Falla, et al. Eur J Pain. 2013 Jull et al. Pain. 2007

0

10

20

30

40

50

60

70

80

90

% R

ed

uc

tio

n in

Ne

ck

Pa

in

Resistance

47%

% R

ed

uc

tio

n in

Ne

ck

Pa

in

25%

MODERATE SEVERE

IDIOPATHIC

COLD HYPERALGESIA

WHIPLASH

16%

% R

ed

uc

tio

n in

Ne

ck

Pa

in

0

10

20

30

40

50

60

70

80

90

14

Numerous clinical trials have demonstrated the efficacy of interventions that target

rehabilitation of sensorimotor control for the management of neck pain

These interventions are more effective when targeted to findings of a detailed assessment

and that people with features consistent with nociceptive pain (e.g. features of pain that

imply a proportional and predictable relationship to mechanical loading) are

more likely to respond favorably

The relative involvement of sensorimotor, psychosocial, and other biological mechanisms

in a patient’s presentation will vary between

individuals and it is not possible to completely separate these mechanisms

A goal is to identify individuals who will benefit

most from rehabilitation targeted at restoration/rehabilitation of sensorimotor

changes and the best methods to address the

underlying mechanisms in those for whom it is relevant