This study demonstrated for the first time that cortical CNV potentials were evident prior to postural perturbations and that modulation of these potentials with changes in central set correlates with modifications of the ensuing postural responses (but not with the anticipatory modifications of initial posture observed prior to the perturbation).
Although CNV potentials appeared not to be present in the No Cue condition, we speculate that this does not represent a complete lack of anticipation and preparation for the postural response, rather that the lack of average potential represents an inconsistently timed anticipation and preparation for the response. That is, we suspect that the subjects always attempted to anticipate the onset of the perturbation, but without the benefit of the predictably timed visual warning cue in the No Cue condition, the subjects were unable to temporally couple their cortical preparation with the perturbation. Thus, over separate trials in the No Cue condition, the subjects’ CNV potentials likely occurred at different times prior to the perturbation and, over repeated trials, these potentials would progressively offset each other in the average EEG waveform. This speculation is consistent with previous studies demonstrating that decreased potential amplitudes correspond to an increased difficulty in predicting response timing when testing subjects under different preparatory periods (McAdam et al., 1969
; Maeda and Fujiwara, 2007
). In contrast, during the Cue condition, the subjects could consistently couple their response preparation with the perturbation and, consequently, their average EEG potentials progressively increased with repeated trials.
The presence of the warning cue not only affected cortical activity, but also affected the magnitude of the subjects’ postural responses: the warning cue resulted in smaller peak CoP excursions that remained farther from the front edge of foot support, as well as fewer unintended steps. These cue-related effects were evident regardless of the order in which the conditions were presented, suggesting that the cue itself – not the order in which the conditions occurred – mediated the subjects’ modifications of their postural responses. Despite the consistent effect of cueing on the subjects’ CoP displacements, no significant differences in joint displacements or EMG activations were evident between the Cue and No Cue conditions. The lack of a significant difference in the subjects’ kinematics and EMG activations seemed to reflect the inter-subject variability in the response strategy used to decrease CoP displacements. This variability in postural strategy is not surprising given that our instructional set was simply to ask the subjects to maintain standing balance with their feet in place, without suggesting a type of strategy to accomplish this goal. Unlike specific joint motions or EMG activations, the reduced CoP excursion represents a generalized measure that reflected the general goal to maintain balance without stepping.
CNV potentials were not evident in the No Perturbation condition, confirming the interpretation that these potentials represented anticipation and motor preparation for the postural response, not solely a visual orienting response. Further, CoP displacements remained farther from the front edge of the subjects’ feet in the Cue condition than in the No Cue condition throughout all 40 trials of each condition, without any evidence of trial-related learning. Thus, the warning cue effectively altered postural performance without the need for practice.
The subjects’ cue-related modifications of their postural responses were related to the cue-related changes in their pre-perturbation cerebral activity. Further, the change in magnitude of the CNV potentials appeared to specifically relate to the modification of the feet-in-place postural response, not the stepping response, because the relationship between response modification and cortical modulation strengthened when removing trials with unintentional steps from the analysis. One outlying subject exhibited an unusually large CNV potential in the No Cue condition after removing trials with steps, and this large potential was likely because the subject was only able to perform 6 of the 40 trials without stepping in the No Cue condition. Thus, when removing trials with unintended steps, this subject’s average CNV potential was not based on enough trials to sufficiently increase the signal-to-noise ratio in order to accurately record the amplitude of the CNV potential.
Although the subjects modified their muscle activity and CoP positions before perturbation onset, most of these modifications were evident in both the Cue and No Cue conditions. For those changes that were different among the Cue and No Cue conditions, these cue-related modifications in initial posture were not related to the subjects’ cue-related modulation of CNV potentials or to the cue-related modification of their CoP responses to the perturbations. Thus, the subjects’ cortical activity prior to the perturbations appears to be related to modifying the postural response directly, rather than indirectly through modifications in initial posture or muscle activity.
It remains unclear whether the pre-perturbation cortical activity modified the postural responses by changing the response strategy or simply by priming and augmenting existing synergies. Previous studies examining the predictability of perturbation onset on postural responses suggest that the response strategy isn’t changed, but simply primed for an earlier response latency (Ackermann et al., 1991
). The original study of CNV potentials (Walter et al., 1964
) also suggested a similar role for the CNV potential, stating that the CNV represents an “electrical sign of cortical priming whereby responses to associated stimuli are economically accelerated and synchronized”, and a recent report on voluntary postural control in response to startle stimuli seems to confirm this interpretation (MacKinnon et al., 2007
). Further study, however, is required to more directly test the contribution of the CNV potential to changes in an intended response strategy, particularly given the constraints we imposed on the subjects’ ability to step or to use their arms in response to the perturbation.
The cerebral cortex may only relate to postural responses when actively attending to postural preparation because both CNV potentials and postural responses depend on a subject’s attention to the movement task (Tecce, 1972
; Norrie et al., 2002
). Because CNV potentials prior to cued responses are dependent on attention to the cue and include a component that is specifically related to a visual orientation to the warning cue (Tecce, 1972
; Kok, 1978
), the results suggest that the activation of cortical circuits to modify postural responses may only occur in situations where a loss of balance is anticipated. Such a contribution, however, would still be essential to human behavior outside the laboratory because individuals can often anticipate potential perturbations based on environmental cues, such as when approaching obstacles or slippery surfaces, when riding public transit, or when participating in sports.
In addition, our study only examined responses to a single type of perturbation, and unpredictable perturbation characteristics may hinder the effectiveness of anticipatory cortical activity to modify a postural response in a context-appropriate manner. Behavioral evidence, however, suggests that healthy subjects are capable of modifying their postural responses through pre-planning based on prior intention or the existence of environmental obstacles, even when responding to perturbations of unpredictable direction, timing, and amplitude (Zettel et al., 2005
; Jacobs and Horak, 2007b
). Nevertheless, further study is required to understand the role of the cerebral cortex in shaping reactive postural responses to unexpected or unpredictable perturbations.
Because a high-density electrode set was unavailable for source analysis in this study, we cannot confirm the cortical generators responsible for modifying postural responses based on changes in central set. However, subdural recordings of CNV potentials during voluntary finger extensions have demonstrated that the neural generators of the CNV potential comprise an executive circuit that includes the prefrontal and temporal cortex, and a motor circuit that includes the supplementary motor area and primary sensory-motor cortex (Lamarche et al., 1995
; Hamano et al., 1997
; Bares et al., 2007
). Thus, given the similarity among the CNV potentials observed in our study and those observed with voluntary movements, we speculate that these neural networks were also involved in modifying the postural responses of the subjects in this study.
This speculation that the observed cortical activity contributes to the modification of ensuing postural responses also insinuates a causal relationship among the pre-perturbation CNV activity and the observed modifications of the postural response. This study, however, only satisfies some of requirements for a causal association: the changes in cortical activity correlate with the changes in the postural response, the cortical activity occurs prior to the postural response, and the potential confound or modifier of pre-perturbation changes in initial posture did not likely explain this relationship. Nevertheless, this study did not examine all the variables with potential to confound the correlation, nor does it demonstrate that changes in cortical activity are necessary for the modification of postural responses with changes in central set.
In summary, our study demonstrated that activity of the cerebral cortex associates with the modification of postural responses to external perturbations through changes in anticipatory central set. Thus, this study adds to a growing literature, demonstrating that postural responses may be influenced by the activity of the cerebral cortex, such as for the identification and sensory-motor processing of postural instability (Slobounov et al., 2005
; Adkin et al., 2006
), modification of postural responses through cortical response loops (Jacobs and Horak, 2007a
; Maki and McIlroy, 2007
), and now through the priming of postural responses before an anticipated perturbation. This literature suggests that movements once considered automatic might be susceptible to voluntary control. Thus, techniques that are used to train voluntary movements (e.g., repetitive training and visualization techniques) may also be useful to train postural responses because the voluntary motor networks of the cerebral cortex access the automated postural networks activated during postural responses. Therefore, individuals with impaired balance may benefit from cognitive training of their postural responses to improve balance control (Rogers et al., 2003
; Jobges et al., 2004
; Maffiuletti et al., 2005
; Woollacott et al., 2005