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To select one hand while using both: neural mechanisms supporting flexible hand dominance in bimanual object manipulation
Umeå University, Faculty of Medicine, Integrative Medical Biology, Physiology. (Roland S Johansson)
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In daily activities, the brain regularly assigns different roles to the hands dependingon task and context. Yet, little is known about the underlying neural processes. Thiscertainly applies to how the brain, where each hemisphere primarily controls onehand, manages the between-hand coordination required in bimanual objectmanipulation. By using behavioral, neurophysiological and functional magneticresonance imaging techniques, the present thesis examines neural mechanisms thatsupport hand coordination during tasks where the two hands apply spatiotemporallycoupled but opposing forces for goal attainment, e.g., as when removing the cap froma bottle. Although the two hands seem to operate symmetrically in such tasks, Study Ishowed that one hand primarily acts while the other assists. Moreover, this roledifferentiation was found to be flexible with the brain appointing either hand asprime actor depending on the spatial congruency between hand forces and desiredmovement consequences. Accordingly, when we remove a cap from a bottle, the handthat grasps the cap, be it left or right depending on overall task constraints, isappointed as prime actor because the twist forces it generates are aligned with thegoal to remove the cap, while the other hand, holding the bottle, applies stabilizingforces in the opposite direction. Changes in hand assignments are caused by amidline shift of lateralized activity throughout the motor system, from distal handmuscles to corticospinal pathways and primary sensorimotor and cerebellar corticalareas (Study I). Although the bimanual actions examined involved both within- andbetween-hand coordination, Study II failed to reveal additional brain activity duringbimanual as compared to matching unimanual actions, except for the primarysensorimotor areas where subpopulations of neurons were preferentially engagedduring either bimanual or unimanual actions. Thus, dedicated neurons in the motorcortices might support critical bimanual coordinative operations. While imagingresults indicated that a mainly left-lateralized parietal-premotor network managedthe task irrespective of prime actor, premotor areas presumably established handassignment by allocating the lead either to the left or the right primary sensorimotorareas (Study I and II). Regarding the process of prime actor selection and hence thecontrol of these premotor networks, imaging results indicate a transitory involvementof prefrontal cortical areas (Study III). The detected areas belong to a networkconsidered critical for cognitive operations such as judgment and decision-making,and for evaluation of utility of actions, including conflict detection. The implicitselection of prime actor during bimanual tasks thus seems to be supported by corticalareas traditionally associated primarily with complex cognitive challenges.

Place, publisher, year, edition, pages
Umeå: Umeå university , 2009. , 41 p.
Series
Umeå University medical dissertations, ISSN 0346-6612 ; 1300
Keyword [en]
object manipulation, bimanual coordination, action selection, cerebral cortex, functional laterality, humans, hand, magnetic resonance imaging, transcranial magnetic stimulation, electromyography
National Category
Physiology
Research subject
Physiology
Identifiers
URN: urn:nbn:se:umu:diva-29805ISBN: 978-91-7264-873-9 (print)OAI: oai:DiVA.org:umu-29805DiVA: diva2:278119
Public defence
2009-12-17, BiA201, Biologihuset, Umeå universitet, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2009-11-26 Created: 2009-11-24 Last updated: 2010-01-18Bibliographically approved
List of papers
1. How a lateralized brain supports symmetrical bimanual tasks
Open this publication in new window or tab >>How a lateralized brain supports symmetrical bimanual tasks
Show others...
2006 (English)In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 4, no 6, e158- p.Article in journal (Refereed) Published
Abstract [en]

A large repertoire of natural object manipulation tasks require precisely coupled symmetrical opposing forces by both hands on a single object. We asked how the lateralized brain handles this basic problem of spatial and temporal coordination. We show that the brain consistently appoints one of the hands as prime actor while the other assists, but the choice of acting hand is flexible. When study participants control a cursor by manipulating a tool held freely between the hands, the left hand becomes prime actor if the cursor moves directionally with the left-hand forces, whereas the right hand primarily acts if it moves with the opposing right-hand forces. In neurophysiological (electromyography, transcranial magnetic brain stimulation) and functional magnetic resonance brain imaging experiments we demonstrate that changes in hand assignment parallels a midline shift of lateralized activity in distal hand muscles, corticospinal pathways, and primary sensorimotor and cerebellar cortical areas. We conclude that the two hands can readily exchange roles as dominant actor in bimanual tasks. Spatial relationships between hand forces and goal motions determine hand assignments rather than habitual handedness. Finally, flexible role assignment of the hands is manifest at multiple levels of the motor system, from cortical regions all the way down to particular muscles.

National Category
Neurosciences
Identifiers
urn:nbn:se:umu:diva-12527 (URN)10.1371/journal.pbio.0040158 (DOI)16669700 (PubMedID)
Available from: 2008-01-11 Created: 2008-01-11 Last updated: 2014-07-18Bibliographically approved
2. Zones of bimanual and unimanual preference within human primary sensorimotor cortex during object manipulation
Open this publication in new window or tab >>Zones of bimanual and unimanual preference within human primary sensorimotor cortex during object manipulation
2007 (English)In: NeuroImage, ISSN 1053-8119, Vol. 36, no Suppl 2, T2-T15 p.Article in journal (Refereed) Published
Abstract [en]

We asked which brain areas are engaged in the coordination of our hands in dexterous object manipulations where they cooperate for achieving a common goal. Well-trained right-handers steered a cursor on a screen to hit successively displayed targets by applying isometric forces and torques to a rigid tool. In two bimanual conditions, the object was held freely in the air and the hands thus generated coupled opposing forces. Yet, depending on the mapping rule linking hand forces and cursor movements, all subjects selected either the left or the right hand as prime actor. In two unimanual conditions, the subjects performed the same task with either the left or the right hand operating on a fixed tool. Functional magnetic resonance imaging revealed common activation across all four conditions in a dorsal fronto-parietal network biased to the left hemisphere and in bilateral occipitotemporal cortex. Contrary to the notion that medial wall premotor areas are especially active in complex bimanual actions, their activation depended on acting hand (left, right) rather than on grip type (bimanual, unimanual). We observed effects of grip type only in the primary sensorimotor cortex (SMC). In particular, with either hand as prime actor, bimanual actions preferentially activated subregions of the SMC contralateral to the acting hand. A sizeable subregion with preference for unimanual activity was found only in the left SMC in our right-handed subjects. Collectively, these results indicate a hemispheric asymmetry for the SMC and that partially different neural populations support the control of bimanual versus unimanual object manipulations.

Identifiers
urn:nbn:se:umu:diva-22644 (URN)10.1016/j.neuroimage.2007.03.042 (DOI)17499166 (PubMedID)
Available from: 2009-05-14 Created: 2009-05-14 Last updated: 2009-11-27Bibliographically approved
3. Selection of prime actor in bimanual object manipulation
Open this publication in new window or tab >>Selection of prime actor in bimanual object manipulation
(English)Manuscript (preprint) (Other academic)
Keyword
object manipulation, bimanual coordination, brain mapping, humans, laterality, cerebral cortex, functional magnetic resonance imaging, decision making, action selection, hand selection
National Category
Physiology
Research subject
Physiology
Identifiers
urn:nbn:se:umu:diva-29804 (URN)
Available from: 2009-11-24 Created: 2009-11-24 Last updated: 2009-11-27Bibliographically approved

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