Organisation of the motor cortex differs between people with and without knee osteoarthritis

Shanahan et al. Arthritis Research & Therapy (2015) 17:164 DOI 10.1186/s13075-015-0676-4 RESEARCH ARTICLE Open Access Organisation of the motor cortex differs between people with and without knee osteoarthritis Camille J. Shanahan1,2, Paul W. Hodges3, Tim V. Wrigley1, Kim L. Bennell1 and Michael J. Farrell2,4* Abstract Introduction: The aim of this study was to investigate possible differences in the organisation of the motor cortex in people with knee osteoarthritis (OA) and whether there is an association between cortical organisation and accuracy of a motor task. Methods: fMRI data were collected while 11 participants with moderate/severe right knee OA (6 male, 69 ± 6 (mean ± SD) years) and seven asymptomatic controls (5 male, 64 ± 6 years) performed three visually guided, variable force, force matching motor tasks involving isolated isometric muscle contractions of: 1) quadriceps (knee), 2) tibialis anterior (ankle) and, 3) finger/thumb flexor (hand) muscles. fMRI data were used to map the loci of peak activation in the motor cortex during the three tasks and to assess whether there were differences in the organisation of the motor cortex between the groups for the three motor tasks. Root mean square of the difference between target and generated forces during muscle contraction quantified task accuracy. Results: A 4.1 mm anterior shift in the representation of the knee (p = 0.03) and swap of the relative position of the knee and ankle representations in the motor cortex (p = 0.003) were found in people with knee OA. Poorer performance of the knee task was associated with more anterior placement of motor cortex loci in people with (p = 0.05) and without (p = 0.02) knee OA. Conclusions: Differences in the organisation of the motor cortex in knee OA was demonstrated in relation to performance of knee and ankle motor tasks and was related to quality of performance of the knee motor task. These results highlight the possible mechanistic link between cortical changes and modified motor behavior in people with knee OA. Introduction Along with pain and changes to knee joint tissues (cartilage, bone, ligaments, muscles and joint capsule), changes in sensory and motor function of the knee are common in people with knee osteoarthritis (OA) [1], yet the underlying mechanisms are not completely understood. It is possible that these changes may be mediated by alteration to the motor regions of the cortex of the brain. Most people with knee OA symptoms experience some degree of impaired motor function [2, 3]. Changes in motor control in knee OA include: alterations to gait and muscle activation patterns [4, 5], quadriceps muscle weakness [6] and impaired proprioception [7]. Altered * Correspondence: 2 The Florey Institute of Neuroscience and Mental Health, Kenneth Myer Building, 30 Royal Parade, Parkville, VIC 3052, Australia 4 Department of Medical Imaging and Radiation Sciences, Monash University, Melbourne, Australia Full list of author information is available at the end of the article organisation of the motor and sensory regions of the cerebral cortex accompanies modified motor control in a range of other musculoskeletal conditions such as recurrent low back pain [8, 9], lateral epicondylalgia [10] and focal hand dystonia [11]. Differing organisation of the brain motor region associated with knee OA is plausible for a number of reasons: 1) the fundamental role of cortical motor regions for the control of movement (including control of basic functions such as gait [12]), 2) the relationship between motor cortex changes and modified behaviour [8], 3) the spectrum of changes to motor control in knee OA [4–7] and, 4) the presence of motor cortex changes in other musculoskeletal conditions [8–11]. To the best of our knowledge there have been no previous studies examining the organisation of the motor cortex in people with knee OA. The adult brain maintains the ability to reorganise in response to activity, injury, stimulation or learning [13]. Reorganisation of the brain involves neural plasticity, which © 2015 Shanahan et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise credited. Shanahan et al. Arthritis Research & Therapy (2015) 17:164 refers to capacity of the nervous system to change morphologically and/or functionally in association with changes in experience [13, 14], although the cause and effect relationship between brain changes and changes in experience is not always clear. In people with knee OA, the changes to motor control constitute significant changes to experience, which could involve brain reorganisation. Reorganisation within the somatosensory and/or motor cortex is often characterised by changes to the somatotopic representation in the sensory and/or motor homunculi [13]. Such reorganisation has been characterised by contraction or expansion of the representation of the affected body part, accompanied by the contraction, expansion or overlap of adjacent representations of other body parts [15, 16]. Expansion of the face representation into the contracted hand representation following hand amputation is an example of this [15, 16]. Somatotopic reorganisation has also been demonstrated in back and upper limb pathologies as overlap between the normally discrete areas of motor cortex that control upper limb [10] or back muscles [17]. In general, there is minimal or no reorganisation of cortical representations at sites that control separate functions and are spatially separated from the primary affected area [18–20]. Although the knee is the primary site of changes to motor control in knee OA, many features of the adapted motor control involve complex functions with interaction between multiple body segments. Reorganisation of motor cortex representations of adjacent lower limb segments, but not the upper limb, is plausible. Functional magnetic resonance imaging (fMRI) of brain activity has been used extensively to investigate organisation and reorganisation of the motor cortex and other areas of the brain related to a range of neurological and orthopaedic conditions [14]. fMRI evaluates neural activity from change in blood flow related to the energy use of neurons using the blood oxygenation level dependent (BOLD) signal [21]. Differences in BOLD signal have been observed with neuroplastic changes related to experience [13, 14], such as following limb amputation [15, 16], and provides an ideal method to study potential changes in brain activity in knee OA. The relevance of differences in brain organisation for motor function depends on identification (...truncated)