Research reportFeedback-dependent modulation of isometric force control: an EEG study in visuomotor integration
Introduction
Research examining the influence of exteroceptive information such as tactile, haptic and visual stimulation upon the control of human movement is well documented [6], [18], [19]. However, the type and nature of the cortical mechanisms underlying the reception and evaluation of these various types of sensory information during movement control is less understood [21], [37], [38]. This is especially evident regarding the lack of research that varies specifically the type and/or amount of visual feedback provided during movement execution [43].
Some of the early work manipulating vision in movement tasks began with studies examining visual-motor tracking and is accrued in a text by Poulton [33]. Much of this research was designed around developing human–machine interfaces. Many features of visual feedback (e.g., control signal order, gain, noise, etc.) were manipulated systematically in order to develop and configure the most optimal visual-motor devices for human controllers.
Although limited in number, this same concept has been applied recently in studies attempting to understand how the central nervous system uses visual information for feedback-based control of movement. Various permutations ranging from control signal gain (also referred to as scale) [4], [5], [10], [20], [21], to delays [12], [28] to the frequency [43] of feedback have been examined. Measures of performance accuracy and movement structure (as assessed via the fast Fourier transform) vary specifically with (i) the type of information provided and (ii) the amount of time allotted for subjects to ‘adapt’ to these variations. Others have illustrated that the amount (gain) [30] and/or type (deceptive) [27] of visual feedback also interacts significantly with the end-effector(s) used for executing a movement. Together this work illustrates that it is not just the task requirements, the type of visual information provided or the end-effector(s) utilized, independently, that is important but rather it is the consequent interaction between these variables (i.e., the physiological relationship) that determines visuomotor output.
Attempts to understand the cortical mechanisms underlying the aforementioned changes in movement performance under various visual feedback scenarios to our knowledge have never been addressed specifically. Recent work, however, does exist that has examined cortical mechanisms during tasks within visuomotor paradigms [7]. Some of these studies have attempted to define the existent neurocognitive strategies – spatially and temporally distinct electrocortical (EEG) patterns – during skill acquisition [50] and under time pressure [46]. Research also exists using other brain imaging modalities (i.e., positron emission tomography) where the focus has been on understanding the visuospatial processing necessary to execute reaching tasks. In general, this work has emphasized the concomitant roles of both the posterior parietal cortex [16], [17], [22] and the premotor and supplementary motor areas [22] during the reach-to-grasp movement sequence.
Experimental paradigms using electroencephalography (EEG) have also been established as a useful tool in examining distinct kinematic and kinetic features of human movement. This has been demonstrated in a series of experiments examining force production [44], [45], rate of force development [39], [44], [48], [49] and the use of various end-effectors [35], [47], [48]. However, none of the aforementioned studies in either visuomotor integration or movement using EEG have manipulated systematically visual feedback.
In this investigation, we attempted to merge two experimentally disparate yet conceptually similar lines of research concerning how changes in visual feedback affect movement control. We examined directly the temporal and spatial properties of cortical excitation (via EEG) while simultaneously evaluating isometric force control under varying levels of precision in visual feedback (control signal gain). Our primary expectation was that subjects would more effectively utilize the additional visual information provided to them in conditions of high control signal gain to improve the accuracy of isometric force output. This increase in visual information coupled with improvements in isometric force accuracy would be mirrored by systematically varied electrocortical patterns observed over the parietal and frontocentral electrode groupings – areas specifically related to multi-modal sensory evaluation (parietal lobe) and higher-order movement control (supplementary and mesial premotor areas), respectively. To our knowledge, this is the first experiment that directly manipulates control-signal gain while simultaneously examining isometric force output and electrocortical patterns in human populations.
Section snippets
Subjects
Seven healthy, self-reported right-hand dominant undergraduate students (four males, three females, mean age: 19.8 years) at the Pennsylvania State University with no reported history of head or hand trauma or neurological disorders participated in this study. All participants had normal and/or corrected vision. Each subject provided informed consent prior to testing. All experimental procedures were approved by the Office of Regulatory Compliance at the Pennsylvania State University.
Grip apparatus
Subjects
Ramp phase
The relative absolute trajectory errors averaged across all subjects for the ramp phase are reported in Table 2. A 2×2 within-subject ANOVA was carried out with the two control-signal gains and the two criterion force levels as factors. There was a significant criterion force effect, P<0.05, F(1,6)=7.74. The post hoc test revealed that the 7.5% condition’s relative absolute trajectory error was significantly greater than the 30%. Neither control-signal gain, P=0.32, F(1,6)=1.15 nor the
Discussion
There is a differential sensitivity of specific cortical regions, as evidenced in the spatial and temporal electrocortical patterns exhibited across the human cortex, to manipulations in the overall magnitude of force and control-signal gain (precision of visual information). This sensitivity is most evident across two regions, the parietal lobe (Pz, P3, P4; Fig. 7, Fig. 8) and the supplementary and mesial premotor areas (FCz; Fig. 7). In addition, these variations in electrocortical patterns
Summary
In general, there is a differential sensitivity of particular cortical areas across various phases of isometric force control to manipulations in the magnitude of force and control-signal gain (precision of visual feedback). Specifically, the interaction between the magnitude of force and control-signal gain observed within the parietal electrode grouping and the effect of control-signal gain observed across the frontocentral electrode grouping, primarily FCz, may be reflective of the
Acknowledgements
The authors would like to thank Marco Santello for valuable comments and suggestions regarding earlier versions of the manuscript.
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