Dynamic shifts in the organization of primary somatosensory cortex induced by bimanual spatial coupling of motor activity
Introduction
Several studies have shown that primary sensory and motor areas are plastic even in the adult age as a consequence of injury or stimulation (e.g., Elbert et al., 1995, Flor et al., 1995, Karl et al., 2001, Merzenich et al., 1983, Yang et al., 1994). In addition, an increasing body of evidence suggests that the functional organization of SI may also change dynamically according to task requirements and context (Braun et al., 2000, Braun et al., 2001, Buchner et al., 1995, Moore et al., 1999, Noppeney et al., 1999).
Both animal studies and human brain mapping studies support the idea of a profound interconnectedness in the sensorimotor system (Kawashima et al., 1993, Pleger et al., 2003, Porter, 1997, Rao et al., 1993). However, the known activation of somatosensory cortex after the execution of a motor task could also be attributed to proprioception (Rausch et al., 1998). Recently, Braun et al. (2001) reported rapid task-specific changes of the organization of SI as a result of motor activity. They showed that cortical representations of D1 and D5 were more distant during handwriting in comparison to rest. Braun et al. could not distinguish whether these changes in the functional organization during movement represented the consequence of altered reafferent input from joints, muscles, and skin during the execution of the motor task or a task-related influence of motor and premotor areas upon the organization of the somatosensory cortex.
In order to test the hypothesis of a task-related influence of motor and premotor areas upon the somatosensory cortex, we investigated the functional organization of SI by applying a standard test used to examine coupling effects that arise when subjects produce bimanual movements. These coupling effects are known to be related to an activation of the premotor cortex and the supplementary motor area (SMA) (Sadato et al., 1997, Steyvers et al., 2003). Participants are asked to cyclically produce trajectories with both hands. The direction of these trajectories is varied to be either the same (parallel) or different (orthogonal). In the parallel condition, the trajectories drawn by each hand are minimally affected in comparison to when either hand performs alone. When the task requires movements in orthogonal directions, both trajectories deviate from their target paths (Franz, 1997, Franz et al., 1991). We assessed the functional topographic organization of somatosensory cortex of the dominant hand during the parallel and the orthogonal condition and a rest state by neuromagnetic source imaging.
Based on the findings of Sadato et al. (1997) and Steyvers et al. (2003), we expected higher activation of the SMA and premotor cortex during the performing of the orthogonal task because this task demands much higher bimanual coordination. Thus, hypothesizing a task-related influence of motor and premotor areas upon the organization of the somatosensory cortex, it was assumed that the pattern of activation of somatosensory cortex changes during the orthogonal condition compared to the parallel and rest condition.
Section snippets
Participants
Ten right-handed, healthy volunteers (all females) with a mean age of 24 years (SD 3.6, range 19–28 years) participated in the study. All subjects were right-handed as assessed by the Edinburgh Handedness Inventory (Oldfield, 1971). The study was adhered to the Declaration of Helsinki and approved by the local human subjects committee. Informed consent was obtained from all subjects.
Procedure and task
During the experiment, subjects were seated on a comfortable chair inside a magnetically shielded room with their
Behavioral performance
The subjects performed the tasks without difficulties. The trajectory of lines became elliptical when the other hand produced circles concurrently but not when the other hand produced lines like the dominant hand (Franz et al., 1991) (Fig. 1). An ANOVA for changes of this displacement revealed a significant main effect for condition (F(1;9) = 47.61, P = 0.0001). Post hoc t tests showed a significant increase of the displacements during orthogonal movements (3.18 ± 1.20 cm) compared to parallel
Discussion
The subjects of this study received tactile stimulation of D1 and D5 of the dominant hand while they were performing simple movements with both hands. The dominant hand always performed the same movement, while the nondominant hand performed the same movement in the parallel condition and a different movement in the orthogonal condition. Thus, identical stimulation was delivered to D1 and D5 of the dominant hand. In addition, subjects were blindfolded; hence, they did not receive visual
Acknowledgment
Supported by DFG grant SCHA1005/1-1 to MS.
References (37)
- et al.
Functional organization of primary somatosensory cortex depends on the focus of attention
NeuroImage
(2002) - et al.
Short-term changes of finger representation at the somatosensory cortex in humans
Neurosci. Lett.
(1995) - et al.
Spatial topological constraints in a bimanual task
Acta Psychol.
(1991) - et al.
Changes of somatosensory evoked potentials during writing with the dominant and non-dominant hands
Brain Res.
(1999) - et al.
Effects of movement and movement imagery on somatosensory evoked magnetic fields following posterior tibial nerve stimulation
Brain Res., Cogn. Brain Res.
(1997) - et al.
Regional cerebral blood flow changes of cortical motor areas and prefrontal areas in humans related to ipsilateral and contralateral hand movement
Brain Res.
(1993) - et al.
Dynamics of neuronal processing in rat somatosensory cortex
Trends Neurosci.
(1999) The assessment and analysis of handedness: the Edinburgh Inventory
Neuropsychologia
(1971)- et al.
Task-relevant modulation of contralateral and ipsilateral primary somatosensory cortex and the role of a prefrontal-cortical sensory gating system
NeuroImage
(2002) - et al.
Directional interference during bimanual coordination, is interlimb coupling mediated by afferent or efferent processes
Behav. Brain Res.
(2003)
Proprioceptive modulation of somatosensory evoked potentials during active or passive finger movements in man
J. Neurol. Neurosurg. Psychiatry
Differential activation in somatosensory cortex for different discrimination tasks
J. Neurosci.
Dynamic organization of the somatosensory cortex induced by motor activity
Brain
Lesions in supplementary motor area interfere with a monkey's performance of a bimanual coordination task
Neurosci. Lett.
Supplementary motor area of the monkey's cerebral cortex, short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section
J. Neurosci.
Increased cortical representation of the fingers of the left hand in string players
Science
Phantom limb pain as a perceptual correlate of massive reorganization in upper limp amputees
Nature
Spatial coupling in the coordination of complex actions
Q. J. Exp. Psychol.
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