Literature DB >> 32579409

The neural foundations of handedness: insights from a rare case of deafferentation.

S A L Jayasinghe1, F R Sarlegna2, R A Scheidt3,4, R L Sainburg1,5.   

Abstract

The role of proprioceptive feedback on motor lateralization remains unclear. We asked whether motor lateralization is dependent on proprioceptive feedback by examining a rare case of proprioceptive deafferentation (GL). Motor lateralization is thought to arise from asymmetries in neural organization, particularly at the cortical level. For example, we have previously provided evidence that the left hemisphere mediates optimal motor control that allows execution of smooth and efficient arm trajectories, while the right hemisphere mediates impedance control that can achieve stable and accurate final arm postures. The role of proprioception in both of these processes has previously been demonstrated empirically, bringing into question whether loss of proprioception will disrupt lateralization of motor performance. In this study, we assessed whether the loss of online sensory information produces deficits in integrating specific control contributions from each hemisphere by using a reaching task to examine upper limb kinematics in GL and five age-matched controls. Behavioral findings revealed differential deficits in the control of the left and right hands in GL and performance deficits in each of GL's hands compared with controls. Computational simulations can explain the behavioral results as a disruption in the integration of postural and trajectory control mechanisms when no somatosensory information is available. This rare case of proprioceptive deafferentation provides insights into developing a more accurate understanding of handedness that emphasizes the role of proprioception in both predictive and feedback control mechanisms.NEW & NOTEWORTHY The role of proprioceptive feedback on the lateralization of motor control mechanisms is unclear. We examined upper limb kinematics in a rare case of peripheral deafferentation to determine the role of sensory information in integrating motor control mechanisms from each hemisphere. Our empirical findings and computational simulations showed that the loss of somatosensory information results in an impaired integration of control mechanisms, thus providing support for a complementary dominance hypothesis of handedness.

Entities:  

Keywords:  complementary dominance; lateralization; motor control; proprioception

Mesh:

Year:  2020        PMID: 32579409      PMCID: PMC7474455          DOI: 10.1152/jn.00150.2020

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.974


  50 in total

1.  Handedness and index finger movements performed on a small touchscreen.

Authors:  Tomoko Aoki; Gil Rivlis; Marc H Schieber
Journal:  J Neurophysiol       Date:  2015-12-16       Impact factor: 2.714

2.  Time-varying stiffness of human elbow joint during cyclic voluntary movement.

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Journal:  Exp Brain Res       Date:  1992       Impact factor: 1.972

3.  Internally driven control of reaching movements: a study on a proprioceptively deafferented subject.

Authors:  Fabrice R Sarlegna; Gabriel M Gauthier; Christophe Bourdin; Jean-Louis Vercher; Jean Blouin
Journal:  Brain Res Bull       Date:  2006-03-03       Impact factor: 4.077

4.  The assessment and analysis of handedness: the Edinburgh inventory.

Authors:  R C Oldfield
Journal:  Neuropsychologia       Date:  1971-03       Impact factor: 3.139

5.  Loss of proprioception produces deficits in interjoint coordination.

Authors:  R L Sainburg; H Poizner; C Ghez
Journal:  J Neurophysiol       Date:  1993-11       Impact factor: 2.714

6.  Motor deficits in patients with large-fiber sensory neuropathy.

Authors:  J N Sanes; K H Mauritz; E V Evarts; M C Dalakas; A Chu
Journal:  Proc Natl Acad Sci U S A       Date:  1984-02       Impact factor: 11.205

7.  Rapid elbow flexion in the absence of proprioceptive and cutaneous feedback.

Authors:  R Forget; Y Lamarre
Journal:  Hum Neurobiol       Date:  1987

8.  Handedness can be explained by a serial hybrid control scheme.

Authors:  V Yadav; R L Sainburg
Journal:  Neuroscience       Date:  2014-08-28       Impact factor: 3.590

9.  Manual motor performance in a deafferented man.

Authors:  J C Rothwell; M M Traub; B L Day; J A Obeso; P K Thomas; C D Marsden
Journal:  Brain       Date:  1982-09       Impact factor: 13.501

10.  The effects of unilateral brain damage on visually guided reaching: hemispheric differences in the nature of the deficit.

Authors:  J D Fisk; M A Goodale
Journal:  Exp Brain Res       Date:  1988       Impact factor: 1.972

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  4 in total

1.  Reaction time asymmetries provide insight into mechanisms underlying dominant and non-dominant hand selection.

Authors:  Brooke Dexheimer; Andrzej Przybyla; Terrence E Murphy; Selcuk Akpinar; Robert Sainburg
Journal:  Exp Brain Res       Date:  2022-09-06       Impact factor: 2.064

2.  When the non-dominant arm dominates: the effects of visual information and task experience on speed-accuracy advantages.

Authors:  Brooke Dexheimer; Robert Sainburg
Journal:  Exp Brain Res       Date:  2021-01-02       Impact factor: 1.972

3.  A Lifespan Approach to Balance in Static and Dynamic Conditions: The Effect of Age on Balance Abilities.

Authors:  Giorgia Marchesi; Alice De Luca; Valentina Squeri; Lorenzo De Michieli; Francesco Vallone; Alberto Pilotto; Alessandra Leo; Maura Casadio; Andrea Canessa
Journal:  Front Neurol       Date:  2022-02-21       Impact factor: 4.003

4.  A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination.

Authors:  Jacob E Schaffer; Fabrice R Sarlegna; Robert L Sainburg
Journal:  Neuropsychologia       Date:  2021-07-24       Impact factor: 3.054

  4 in total

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