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Activity-Vs. Structural-Oriented Treatment Approach For Frozen Shoulder: A Randomized Controlled Trial

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63 views10 pages

Activity-Vs. Structural-Oriented Treatment Approach For Frozen Shoulder: A Randomized Controlled Trial

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Isaias Almeida
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© © All Rights Reserved
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687613

research-article2016
CRE0010.1177/0269215516687613Clinical RehabilitationHorst et al.

CLINICAL
Article REHABILITATION

Clinical Rehabilitation

Activity- vs. structural-oriented 2017, Vol. 31(5) 686­–695


© The Author(s) 2017
Reprints and permissions:
treatment approach for frozen sagepub.co.uk/journalsPermissions.nav
DOI: 10.1177/0269215516687613
https://doi.org/10.1177/0269215516687613

shoulder: a randomized journals.sagepub.com/home/cre

controlled trial

Renata Horst1, Tomasz Maicki2,3, Rafał Trąbka2,3,


Sindy Albrecht4, Katharina Schmidt5, Sylwia Mętel6
and Harry von Piekartz7

Abstract
Objective: To compare the short- and long-term effects of a structural-oriented (convential) with an
activity-oriented physiotherapeutic treatment in patients with frozen shoulder.
Design: Double-blinded, randomized, experimental study.
Setting: Outpatient clinic.
Subjects: We included patients diagnosed with a limited range of motion and pain in the shoulder
region, who had received a prescription for physiotherapy treatment, without additional symptoms of
dizziness, a case history of headaches, pain and/or limited range of motion in the cervical spine and/or
temporomandibular joint.
Interventions: The study group received treatment during the performance of activities. The comparison
group was treated with manual therapy and proprioceptive neuromuscular facilitation (conventional
therapy). Both groups received 10 days of therapy, 30 minutes each day.
Main measures: Range of motion, muscle function tests, McGill pain questionnaire and modified Upper
Extremity Motor Activity Log were measured at baseline, after two weeks of intervention and after a
three-month follow-up period without therapy.
Results: A total of 66 patients were randomized into two groups: The activity-oriented group (n = 33,
mean = 44 years, SD = 16 years) including 20 male (61%) and the structural-oriented group (n = 33, mean =
47 years, SD = 17 years) including 21 male (64%). The activity-oriented group revealed significantly greater
improvements in the performance of daily life activities and functional and structural tests compared with
the group treated with conventional therapy after 10 days of therapy and at the three-month follow-up
(p < 0.05).

1Private 6Department of Physical Medicine and Biomedical Renewal,


Practice and Institute for Further Education for
Medical Professions, Ingelheim, Germany University of Physical Education in Krakow, Cracow, Poland
2Clinic of Rehabilitation, Jagiellonian University, Cracow, 7University of Applied Science, Hochschule Osnabruck Fakultat

Poland Wirtschafts- und Sozialwissenschaften, Osnabrueck, Germany


3Cracow Rehabilitation Center, Cracow, Poland
4Leuphana University, Lüneburg, Germany Corresponding author:
5Department of Sports Medicine, Goethe-University, Renata Horst, Private Practice, Stiegelgasse 40, Ingelheim
55218, Germany.
Frankfurt am Main, Germany
Email: [email protected]
Horst et al. 687

Conclusions: Therapy based on performing activities seems to be more effective for pain reduction and
the ability to perform daily life activities than conventional treatment methods.

Keywords
Shoulder, pain, manual therapy, proprioceptive neuromuscular facilitation, neuro-orthopaedic activity-
dependent plasticity, motor learning

Received: 30 August 2015; accepted: 11 December 2016

Introduction
Patients with frozen shoulder generally suffer a and published in a Cochrane review, which showed
great deal of pain, which often causes prolonged that the efficacy of conventional physiotherapy, as
limitations in performance of daily activities and in the first line of treatment for shoulder pain, has not
participation in socio-cultural life. The prevalence been established.6 Passive mobilization techniques
of frozen shoulder is estimated to be 2% to 5% of may even be harmful for the glenohumeral joint.7
the general population. It is more prevalent in Up to now, studies comparing two different physio-
women and middle-aged to older people, and the therapeutic interventions have not been able to
non-dominant shoulder is slightly more likely to be demonstrate significant differences in outcomes.
affected. In general, the term frozen shoulder is Short-term increases in range of motion did not cor-
used for both primary adhesive capsulitis as well as relate with improvement in quality of life. No stud-
secondary frozen shoulder.1 ies have been found that included the patient’s
Feeling pain, often accompanied with fear of subjective evaluation. Consequently, no conclusions
pain or body injury, causes activity avoidance can be drawn pertaining to cost-efficiency for any
(non-use) or ‘freezing’ of the shoulder. One under- specific intervention.8
lying clinical hypothesis is that pain causes learned Numerous studies have shown that learning
non-use, which entails changes in the brain and depends on experience and it is assumed that prac-
therefore, even after healing of periphereal struc- tise that enables experience changes the nervous
tures has occurred, the brain may not be able to system.9–13 How practise is structured determines if
organize voluntary actions owing to the induced consolidation, which is the basis for long-term
central changes.2,3 This raises two questions for learning, will result.14,15 Activity-oriented move-
orthopaedic patients: (1) whether changes in ment strategies depend on cognitive aspects, such
peripheral structures alone or also central changes as memory, experience and intention, as well as
in cortical representation may be responsible for feelings and emotions, which are essential for
limitations, and (2) whether interventions, which memory and learning.16,17
incorporate treatment of body structures during the Considering these facts, the aim of this rand-
performance of activities, may be more effective omized trial is to compare the short- and long-term
for long-term effects and memory than physical effects of a structural-oriented with an activity-
therapy, which emphasizes treatment at the struc- oriented physiotherapeutic treatment.
tural level alone.
Conventional methods for treatment of neuro-
musculoskeletal disorders primarily focus on the
Methods
functioning of body structures, assuming that if joint This double-blinded, randomized, experimental
play is restored and if stiff or contract muscles are study was approved by the Regional Medical Ethics
relaxed and weak muscles strengthened, the ability Board of Physicians in Krakow, Poland (pol.
to perform activities is automatically recovered.4,5 A Okręgowa Izba Lekarska w Krakowie) nr 18/KBL/
total of 26 trials were included for a meta-analysis OIL/2011. We only included patients who had been
688 Clinical Rehabilitation 31(5)

diagnosed with limited range of motion, pain in the Table 1.  Description of activities which were
shoulder region and had received a prescription for assessed.
physiotherapy treatment at the Krakow Rehabilitation Activity 1 Putting on and taking off a t-shirt with
Centre in Krakow, Poland, by an orthopaedic spe- both hands.
cialist. The orthopaedic specialist had more than Activity 2 Placing both hands behind the neck, as
20 years of experience in treatment of these patients. to fasten a necklace.
No limitations pertaining to age and gender were Activity 3 Placing both hands behind the back, as to
made. tie an apron.
Before being enrolled in the study, potential par- Activity 4 Lifting a bottle of 1 L contents onto a shelf
ticipants received oral and written information of 145 cm height with the affected arm.
about the study and had to provide written informed Activity 5 Lifting a case of water containing 9 L with
both hands onto a height of 145 cm.
consent. Following, patients were asked to com-
plete a questionnaire describing their case history
and symptoms to assess eligibility. Patients were
excluded if they had additional symptoms of dizzi- The McGill pain questionnaire and modified
ness and a case history of headaches, pain and/or Upper Extremity Motor Activity Log were used for
limited range of motion in the cervical spine and/or patient’s subjective evaluation (see Appendix 1
temporomandibular joint. Prior to the first treat- and 2, available online).18,19 The Upper Extremity
ment, participants were randomly assigned to one Motor Activity Log, which was developed for
of the two treatment groups by drawing a sealed assessing the capability to perform 30 different
envelope, which entailed either an even or an odd activities of daily living in patients following stroke,
number. Patients who drew an even number were was modified to focus on five relevant daily life
assigned to the activity-oriented group. Those who activities, which patients with frozen shoulder were
drew an odd number were assigned to the struc- not able to perform before therapy onset (Table 1).
tural-oriented group. Tests for range of motion were performed using
One blinded therapist, who had no knowledge a 12-inch plastic BASELINE goniometer, (Model
of which intervention the patients received, per- 12-1000) Fabrication Enterprises (White Plains,
formed all tests. Assessments were done at baseline New York) for all goniometric measurements.20
(before the first intervention), after two weeks The muscle testing procedures from Daniels and
with ten physiotherapy sessions and after three- Worthingham were applied to assess strength of
months follow-up without therapeutic intervention. all major muscles of the shoulder. In this system,
Participants in both groups did not receive any muscle strength is scored with a numerical grading
information about the kind of intervention or treat- system ranging from 0, indicating no muscle acti-
ment they were receiving. vation, to 5 for the best possible response to man-
Four therapists took part in the study. Two thera- ual resistance in a shortened range of the muscle
pists treated their patients at an activity level and group performing the motion.21
the other two therapists treated their patients at a All subjects received a total of 10 therapeutic ses-
structural level. All therapists had a minimum of sions in a time period of two weeks for a duration of
four years practical experience as physiotherapists 30 minutes each. The activity-oriented group (study
after having completed their Master Degrees at the group) was instructed to focus on attaining a relevant
University. The two therapists for the structural- goal during the manual guidance of the therapist with
oriented group had also been certified in further the aim to enable the best possible musculoskeletal
education courses as manual therapists and thera- situation for the required movements.22 The struc-
pists in proprioceptive neuromuscular facilitation. tural-oriented group (comparison group) was treated
The two therapists for the activity-oriented treat- at the structural level according to conventional
ments had been trained in the methods described physical therapy methods: Manual therapy and pro-
later in Table 2. prioceptive neuro-muscular facilitation techniques.4,5
Horst et al. 689

Table 2.  Comparison of methods applied in the activity-oriented treatment (study group) with the methods of the
structural-oriented therapy (comparison group).

Methods of activity-oriented therapy Methods of structural-oriented therapy


1. Randomized practise: For example, training external Blocked practise: For example, practising a
rotators of the shoulder in different situations, such particular PNF pattern to train the external
as rolling from side-lying to supine, sitting back on the rotators of the shoulder until it can be
heels in quadriped, putting on a jacket, with only a few performed before going on to a second
repetitions between the different activities. pattern.
2. Intrinsic feedback: For example, asking the patient how Extrinsic feedback: For example, telling the
he thinks he could control his scapula to avoid pain. patient how to control his scapula motion to
avoid pain.
3. External focus: For example, asking the patient to comb Internal focus: For example, telling the patient
his hair. to lift his arm.
4. Mental and emotional involvement: For example, during Passive mobilization techniques: For example,
sitting back on the heels in quadriped, the humeral head the therapist mobilizes the humeral head in a
is actively mobilized in a ventral direction owing to ventral direction to increase external rotation.
eccentric activation of the Musculus latissimus dorsi.
5. Influencing biomechanics during performance of Tactile input for movement initiation: For
activities: For example, rotating the clavicula dorsally example, passive mobilization of the scapula
and caudally during the activity of putting on a t-shirt in posterior depression to show the patient
over head to enable decompression of the acromo- where to move with successive increase in
clavicular joint. resistance for the scapula depressors.
6. Shaping according to individual potentials and needs: For Fixed sequence of exercises: For example,
example, beginning in standing if necessary to perform beginning in lying positions and successively
the activity of putting on a t-shirt or combing ones hair. going into higher positions.
7. Training distally organized movements together with Training proximal body parts cognitively and
subconsciously controlled proximal ones: For example, separately before distal ones: For example, the
while the patient attempts to grasp an object over therapist gives traction to the humeral head
head the therapist enables joint stability by stimulating and asks the patient to actively pull the humeral
mechanoreceptors in applying pressure upon the head into the glenohyoidal socket or gives
humeral head towards the glenoid fossa. resistance to the angulus inferior asking the
patient to push it downwards.

PNF: proprioceptive neuromuscular facilitation.

Table 2 provides insight to the methods for both an indication of a statistically significant result. No
intervention groups. Both groups received the same adjustment for multiple comparisons was made. All
additional treatment consisting of aerobic training, statistical analyses were performed using R 3.0.23
cryotherapy, laser therapy and resistance band
exercises.
Categorical variables were described using counts
Results
and percentages. The quantitative variables were The study was conducted between 2011 and 2012.
described using median and quartiles (Me [Q1;Q3]), A total of 66 patients were statistically analysed,
mean and SD. The null hypothesis of no difference six patients were excluded (Figure 1). The activity-
concerning changes in all study outcomes between oriented group (n = 33, mean age = 44 years, SD =
groups was tested based on a comparison of change 16 years) included 20 male (61%) and 13 female
scores (ChS) using the Mann–Whitney test. For cat- (39%) patients. The structural-oriented group
egorical variables, statistical significance of differ- (n = 33, mean age = 47 years, SD = 17 years) com-
ences between groups was assessed using the Fisher’s prised 21 male (64%) and 12 female (36%) patients.
exact test. A p-value less than 0.05 was considered as At baseline, groups were comparable concerning
690 Clinical Rehabilitation 31(5)

Figure 1.  Flowchart of study participation.

age and gender distribution as well as all study out- Concerning pain, the activity-oriented group had a
comes (p > 0.05). significantly greater reduction from baseline to the
Table 3 and 4 display the changes in the out- 3-month follow-up than the structural-oriented
come measures after two weeks of intervention group (p < 0.05). With respect to range of motion,
(after 2) and after the 3-month follow-up (after 3). significant group differences in favour of the
In more than half of the outcomes, the activity- activity-oriented group were found for changes in
oriented group experienced significantly greater adduction, and external and internal rotation from
improvements in comparison with the structural- baseline to the second and third assessment
oriented group. (Table 4). Changes in muscle strength of the flex-
Regarding the activities of daily living, a ors, adductors, abductors, internal rotators and
greater percentage of the activity-oriented group external rotators from baseline to the end of the
compared with the structural-oriented group was intervention and to the three-month follow-up
able to perform activities number 4 and 5 after two were significantly higher in the activity-oriented
weeks of intervention and activities number 1, 3 group compared with the structural-oriented group
and 5 at 3-month follow-up (p < 0.05) (Table 3). (p < 0.05) (Table 4).
Horst et al. 691

Table 3.  Group comparisons for the treatment outcomes concerning activities of daily living. (Number and
percentage of patients being able to perform the activity.).

Activity- Structural- p-value


oriented group oriented group

  n = 33 n = 33  
Activity no. 1
 Before 15 (45%) 12 (36%) 0.617
  After 2 29 (88%) 22 (67%) 0.076
  After 3 31 (94%) 22 (67%) 0.011
Activity no. 2
 Before 16 (48%) 17 (52%) 1.000
  After 2 30 (91%) 27 (82%) 0.475
  After 3 31 (94%) 28 (85%) 0.426
Activity no. 3
 Before 16 (48%) 11 (33%) 0.317
  After 2 28 (85%) 21 (64%) 0.090
  After 3 32 (97%) 24 (73%) 0.012
Activity no. 4
 Before 17 (52%) 10 (30%) 0.132
  After 2 29 (88%) 21 (64%) 0.042
  After 3 31 (94%) 25 (76%) 0.082
Activity no. 5
 Before 4 (12%) 3 (9%) 1.000
  After 2 17 (52%) 6 (18%) 0.010
  After 3 25 (76%) 6 (18%) <0.001

Activity-oriented group (study group): patients receiving treatment during the performance of activities; structural-oriented group
(comparison group): patients treated with manual therapy and proprioceptive neuromuscular facilitation.
Treatment outcomes– Before: baseline measurements; After 2: after two weeks of intervention; After 3: follow-up examination
(after three months).
Bold values: p<0.05.

Discussion one. Evidence has demonstrated that experience-


induced changes occur even after short periods of
The present randomized study compared the effects practise.24 Therefore, it may not be necessary to
of a structural-oriented with an activity-oriented mobilize joints passively and to strengthen muscles as
physiotherapeutic intervention. The results of this a preparation for activities. Experiencing successful
study indicate that influencing body structures dur- activities themselves may induce long-term structural
ing the execution of daily life activities is more changes and less pain perception. Since plasticity is
effective than conventional physiotherapeutic meth- dependent on experience and how treatment sessions
ods and has both short-term and especially long- are structured, practising relevant goal-oriented activ-
term effects for reducing pain and enabling the ities while ensuring the best possible musculoskeletal
performance of activities of daily living. situation may enable the patient to perform these
These improvements were not only measured after activities with less pain and herewith regain cortical
10 days of physiotherapy, but also continued during a representation.9–13
follow-up period of three months without therapy. When injury occurs, it is a very effective strat-
These findings suggest that consolidation may be egy to ‘freeze’ the injured body part to enable
significantly better when following an activity- wound healing to occur. For this, the sympathetic
oriented approach rather than a structural-oriented nervous system generates a cascade of biochemical
692 Clinical Rehabilitation 31(5)

Table 4.  Changes in study outcomes showing a comparison of the activity-oriented group with the structural-oriented
group after two weeks of intervention and after three months of treatment compared with baseline measurements.

Outcome Activity- Structural- p-value 95% CI:


oriented group oriented group

Median Median Differences


[Q1;Q3] [Q1;Q3] between medians
Pain ChS
  After 2 −10 [−11;−6] −7 [−9;−6] 0.083 (−4;1)
  After 3 −15 [−17;−10] −10 [−13;−6] 0.005 (−8;−1)
Range of motion
Flexion ChS
  After 2 23 [6;39] 15 [12;24] 0.286 (−8;21)
  After 3 32 [6;48] 18 [12;29] 0.338 (−11;27)
Extension ChS
  After 2 30 [10;40] 20 [0;30] 0.113 (0;20)
  After 3 30 [20;50] 20 [0;30] 0.061 (0;40)
Rotation internal ChS
  After 2 29 [21;43] 14 [8;22] <0.001 (8;24)
  After 3 36 [22;57] 15 [7;36] 0.003 (4;31)
Rotation external ChS
  After 2 25 [17;34] 17 [8;25] 0.025 (0;16)
  After 3 34 [25;59] 25 [16;33] 0.017 (0;25)
Abduction ChS
  After 2 24 [12;35] 18 [12;30] 0.700 (−8;14)
  After 3 29 [12;47] 26 [15;38] 0.386 (−10;21)
Adduction ChS
  After 2 22 [15;41] 15 [11;20] 0.009 (0;17)
  After 3 26 [15;52] 19 [15;27] 0.024 (0;23)
Muscle strength
Flexion ChS
  After 2 30 [10;70] 5 [0;20] 0.001 (10;40)
  After 3 40 [20;80] 10 [0;40] 0.001 (10;70)
Extension ChS
  After 2 30 [0;70] 20 [10;50] 0.990 (−25;20)
  After 3 60 [10;80] 20 [10;70] 0.167 (−30;60)
Rotation internal ChS
  After 2 20 [10;70] 0 [0;10] <0.001 (10;35)
  After 3 40 [10;80] 0 [0;10] <0.001 (15;70)
Rotation external ChS
  After 2 10 [0;30] 5 [0;10] 0.059 (0;15)
  After 3 20 [10;70] 5 [0;10] 0.001 (5;35)
Abduction ChS
  After 2 20 [5;60] 0 [0;10] 0.002 (5;30)
  After 3 20 [5;80] 0 [0;10] <0.001 (10;80)
Adduction ChS
  After 2 20 [5;70] 10 [0;10] 0.010 (0;40)
  After 3 55 [10;90] 10 [10;40] 0.012 (0;70)

Activity-oriented group (study group): patients receiving treatment during the performance of activities; structural-oriented group
(comparison group): patients treated with manual therapy and proprioceptive neuromuscular facilitation; ChS: change score;
CI: confidence interval.
Treatment outcomes – After 2: after two weeks of intervention; After 3: follow-up examination (after three months).
Bold values: p<0.05.
Horst et al. 693

processes, such as protective muscle tone of mus- range of motion, can also be influenced effectively
cles with primary tonic muscle fibres and contrac- by influencing body structures during the perfor-
tion of myofibroblasts within connective tissues.25 mance of activities rather than treating these alone.
As long as injured body structures require immobi- Brain plasticity may be the explanation for the
lization, these protective mechanisms fulfil a positive treatment results rather than plasticity of
meaningful task. If they are kept up longer than peripheral structures alone.
necessary, then this may lead to learned non-use, A limitation to this study is that within the inclu-
loss of cortical representation and finally to stiff- sion criteria no difference was made between
ness, which in turn may cause increased pain and patients with ‘primary frozen shoulder’ (spontane-
again activates the sympathetic system. In order to ous painful contracture of the glenohumeral joint
stop this vicious circle, it appears reasonable that with no distinct causes) and ‘secondary frozen
the patient needs to experience that these protective shoulder’ (caused by rotator cuff ruptures, neuro-
mechanisms are no longer necessary. logical impairments and metabolic disorders, asso-
Application of external tactile stimuli by the ciated with diabetes mellitus).28 Even among the
therapist is fundamental to both, orthopaedic man- ‘secondary frozen shoulder’ patients, it may be
ual therapy and neurophysiological treatment con- worthwhile to study the differences in outcome
cepts. However, conventional therapy concepts, regarding the different causes and stages of pathol-
which follow a stimulus-response approach using ogy. A patient with a metabolic disorder may not
the hands as a tool to initiate movement or to pre- profit from treatment of the structures concerning
pare structures for activities, may not be as effec- the shoulder complex, whereas a patient with a
tive for long-term learning as structuring practise rotator cuff rupture may.
to enable the successful performance of various The duration of therapy, which lasted for only
activities.9,10,16,17 10 days for 30 minutes daily, was specific for the
In neurological rehabilitation, a great amount of rehabilitation centre where the study was carried
research has been done within the past few dec- out. It may be helpful to gain more insight for gen-
ades, which has led to new clinical implications for eral clinical implications by gathering information
neurological patients. Brain research may also help on outcomes for patients who remain in therapy for
to better understand the mechanisms underlying four weeks, with a therapy frequency of two to
the pathologies of orthopaedic patients. Since plas- three times a week as well. A further limitation was
tic changes within the capsule require sufficient owing to the fact that all patients had a medical pre-
force applied to tissues, perhaps stiffness and scription for physiotherapy. Consequently, it was
decreased range of motion were not primarily not possible to assess a non-intervention control
owing to capsule adhesions.26 Since pain is consid- group, but we used conventional physiotherapy as
ered to be subjective and dependent on individual standard treatment for the comparison group.
experience, persisting even if structures are no Nevertheless, since the focus of the study group
longer affected or not even existent, the reduction was at the activity level, it is possible that patients
of pain perception may not have solely been caused who do not receive physiotherapy and have to cope
by treating peripheral body structures.27 The expe- in activities of daily living may have improvements
rience that relevant goals were able to be attained as well. Future studies may need to include patients
with less pain by ensuring the best possible muscu- who have had a case history of shoulder pain and
loskeletal situation during the performance of daily limited range of motion of at least three months
life activities may possibly explain the results of prior to baseline to rule out this assumption.
this study. The question that may require further investiga-
In summary, the clinical implication from these tion is of how much importance it may be to influ-
observations and knowledge from current evidence ence body structures during the execution of
is that practising activities leads to better perfor- voluntary goal-oriented activities to enable posi-
mance of these. Pain reduction, as well as increased tive movement experiences and how relevant this
694 Clinical Rehabilitation 31(5)

may be for better performance of daily life activi- 6. Green S, Buchbinder R and Hetrick SE. Physiotherapy
ties. The consideration of positron emission tomog- interventions for shoulder pain. Cochrane Database
Syst Rev 2003; (2). Art. No.: CD004258. DOI: 10.1002/
raphy may be useful to identify potential changes 14651858.CD004258.
in cortical representation before and after therapy. 7. Donatelli R, Ruivo RM, Thurner M and Ibrahim MI.
Future studies may help to gain insight as to how New concepts in restoring shoulder elevation in a stiff
neuroplasticity may be influenced for better out- and painful shoulder patient. Phys Ther Sport 2014;
come in neuromusculoskeletal disorders and lead 15(1): 3–14.
8. Maund E, Craig D, Suekarran, et al. Management of fro-
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9. Kleim JA and Jones TA. Principles of experience-
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Bäckman L. Structural brain plasticity in adult learning
Acknowledgements and development. Neurosci Biobehav Rev 2013; 37(9 Pt
I wish to thank Topschool Cracow and the staff of the B): 2296–2310.
Cracow Rehabilitation Center in Cracow, Poland, for 13. May A. Experience-dependent structural plasticity in the
adult human brain. Trends Cogn Sci 2011; 15(10): 475–482.
providing patients for this study.
14. Kantak SS, Sullivan KJ, Fischer BE, Knowlton BJ and
Winstein CJ. Neural substrates of motor memory consoli-
Conflict of interest statement dation depend on practice structure. Nat Neurosci 2010;
13: 923–925.
The authors declared no potential conflicts of interest 15. Cross ES, Schmitt PJ and Grafton ST. Neural substrates of
with respect to the research, authorship, and/or publica- contextual interference during motor learning support a model
tion of this article. of active preparation. J Cogn Sci 2007; 19: 1854–1871.
16. Abe M, Schambra HM, Wassermann EM, Luckenbaugh
D, Schweighofer N and Cohen LG. Reward improves
Funding long-term retension of a motor memory through induc-
The authors received no financial support for the tion of offline memory gains. Curr Biol 2011; 21(7):
research, authorship, and/or publication of this article. 557–562.
17. Pignatelli M and Bonci A. Role of dopamine neurons in
reward and aversion: A synaptic plasticity perspective.
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