Right hemisphere brain lateralization for knee proprioception among right-limb dominant individuals

Andrew Strong; Helena Grip; Ashokan Arumugam; Carl-Johan Boraxbekk; Jonas Selling; Charlotte K Häger

doi:10.3389/fnhum.2023.969101

Right hemisphere brain lateralization for knee proprioception among right-limb dominant individuals

Front Hum Neurosci. 2023 Jan 19:17:969101. doi: 10.3389/fnhum.2023.969101. eCollection 2023.

Authors

Andrew Strong¹, Helena Grip², Ashokan Arumugam³, Carl-Johan Boraxbekk^{2

4

5

6

7}, Jonas Selling¹, Charlotte K Häger¹

Affiliations

¹ Department of Community Medicine and Rehabilitation, Physiotherapy, Umeå University, Umeå, Sweden.
² Department of Radiation Sciences, Umeå University, Umeå, Sweden.
³ Department of Physiotherapy, College of Health Sciences, University of Sharjah, Sharjah, United Arab Emirates.
⁴ Danish Research Centre for Magnetic Resonance, Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital Hvidovre, Copenhagen, Denmark.
⁵ Umeå Center for Functional Brain Imaging, Umeå University, Umeå, Sweden.
⁶ Institute of Sports Medicine Copenhagen and Department of Neurology, Copenhagen University Hospital Bispebjerg, Copenhagen, Denmark.
⁷ Institute for Clinical Medicine, Faculty of Medical and Health Sciences, University of Copenhagen, Copenhagen, Denmark.

Abstract

Introduction: Studies indicate that brain response during proprioceptive tasks predominates in the right hemisphere. A right hemisphere lateralization for proprioception may help to explain findings that right-limb dominant individuals perform position matching tasks better with the non-dominant left side. Evidence for proprioception-related brain response and side preference is, however, limited and based mainly on studies of the upper limbs. Establishing brain response associated with proprioceptive acuity for the lower limbs in asymptomatic individuals could be useful for understanding the influence of neurological pathologies on proprioception and locomotion.

Methods: We assessed brain response during an active unilateral knee joint position sense (JPS) test for both legs of 19 right-limb dominant asymptomatic individuals (females/males = 12/7; mean ± SD age = 27.1 ± 4.6 years). Functional magnetic resonance imaging (fMRI) mapped brain response and simultaneous motion capture provided real-time instructions based on kinematics, accurate JPS errors and facilitated extraction of only relevant brain images.

Results: Significantly greater absolute (but not constant nor variable) errors were seen for the dominant right knee (5.22° ± 2.02°) compared with the non-dominant left knee (4.39° ± 1.79°) (P = 0.02). When limbs were pooled for analysis, significantly greater responses were observed mainly in the right hemisphere for, e.g., the precentral gyrus and insula compared with a similar movement without position matching. Significant response was also observed in the left hemisphere for the inferior frontal gyrus pars triangularis. When limbs were assessed independently, common response was observed in the right precentral gyrus and superior frontal gyrus. For the right leg, additional response was found in the right middle frontal gyrus. For the left leg, additional response was observed in the right rolandic operculum. Significant positive correlations were found between mean JPS absolute errors for the right knee and simultaneous brain response in the right supramarginal gyrus (r = 0.464, P = 0.040).

Discussion: Our findings support a general right brain hemisphere lateralization for proprioception (knee JPS) of the lower limbs regardless of which limb is active. Better proprioceptive acuity for the non-dominant left compared with the dominant right knee indicates that right hemisphere lateralization may have meaningful implications for motor control.

Keywords: brain; functional laterality; functional magnetic resonance imaging (fMRI); knee; lower extremities; motion capture; motor control; proprioception.

Grants and funding

This study was funded by the Swedish Research Council (Grant No. 2017-00892); Region Västerbotten (Strategic funding VLL-358901; Project No. 7002795, Cutting Edge funding RV966109, ALF funding RV 967112); the Swedish Research Council for Sport Science (Grant Nos. P2020-0035 and P2021-0061); The Umeå University Foundation for Medical Research; and King Gustaf V and Queen Victoria’s Foundation of Freemasons. The funders did not have any role in study design.