*Correspondence:
This article was submitted to the journal Frontiers in Integrative Neuroscience.
Edited by: Isaac Louis Kurtzer, New York Institute of Technology–College of Osteopathic Medicine, USA
Reviewed by: Colum Doan MacKinnon, University of Minnesota, USA
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The ability to maintain standing balance and orientation is crucial to mobility and independence. Standing balance is generally maintained by anticipatory postural adjustments associated with voluntary actions. However, inaccurate judgment or impaired anticipatory processes, as well as extrinsic postural perturbations–external forces not generated intrinsically due to voluntary movement (e.g., due to a slip, trip, push, etc.)–can render the need for reactive postural control to recover orientation and balance (Fasano et al.,
For people with disorders of posture and balance associated with aging, neurodegeneration, or injury, an appropriately timed and coordinated postural response to extrinsically perturbed balance may represent the crucial difference between a harmless balance recovery and an aggravated pain condition or injurious fall. Indeed, postural responses to slips and sudden changes in load are common circumstances for incurring an episode of low back pain (LBP), a worldwide leading cause of disability (Manning et al.,
A recently proposed neurophysiologic model of extrinsically induced postural responses reviewed initial evidence that the cerebral cortex influences these postural responses by (a) priming the most contextually accurate response during preparation, and (b) modifying late response phases (Jacobs and Horak,
Understanding cortical function associated with impaired postural responses is essential given (a) the important role of the cerebral cortex for generating postural responses, (b) the potential that its influence may be enhanced to compensate for impaired automated processes of sub-cortical control, and (c) the accessibility of cortex for neuroplastic change with intervention. Unfortunately, because postural responses to extrinsic perturbations were historically considered reflexive and indicative of sub-cortical processing, the literature regarding cortical influence on extrinsically induced postural responses is not well developed. Whereas a more longstanding and developed literature exists on the role of the cerebral cortex for generating anticipatory postural adjustments with voluntary movement—both in the use of many methods of neurophysiologic recording and in the evaluation of people with health conditions (Gurfinkel and El'ner,
Therefore, the purpose of this opinion article is to focus on the cortical neurophysiology of impaired human postural responses to extrinsic perturbations of upright stance. This article will highlight the insights provided from rare studies of cortical function in people with impaired standing postural responses in order to demonstrate the need and potential value of future research focused on the cortical neurophysiology of impaired human postural responses to extrinsic perturbations.
Table
Stroke involving cortex | Feet-in-place responses: change in the distal-to-proximal muscle pattern and delayed muscle onset as well as delayed and slowed rates of force development in the more severely involved limb (Di Fabio et al., |
Unaware of studies utilizing measures of cortical neurophysiology during standing postural responses post-stroke |
Stepping responses: paretic limb exhibits delayed foot-lift, low clearance, need for multiple steps, or an inability to initiate a step (Lakhani et al., |
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Advanced age | Age associates with delays and antagonistic co-contraction of muscles, as well as greater displacement and instability (Halicka et al., |
Electroencephalographic (EEG) PEP delayed, bifid (double-peaked), and decreased with age—effects larger in balance impaired elders (Duckrow et al., |
Dual task costs greater for elderly only in late-phase in-place and stepping responses, more so for stepping and more so if balance impaired elder (Brown et al., |
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Parkinson's disease | Falls, instability, antagonistic co-contraction and lack of modulation based on knowledge of perturbation. Stepping responses may exhibit freezing or have decreased velocity and step length (Jacobs et al., |
Increased desynchronization of EEG beta signal, and this increase associates with decreased response adaptation to perturbation magnitude (Smith et al., |
With dual tasking, in-place responses are not modulated, and falls increase during stepping responses, but postural preparation or freezing unchanged (de Lima-Pardini et al., |
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Low back pain | Increased pre-perturbation muscle activation, increased activation amplitude at distal muscle, but decreased or delayed trunk muscle activation (Jacobs et al., |
Late positive peak PEP larger with LBP; larger PEP correlates with less postural instability, disability, and fear of activity (Jacobs et al., |
Unfortunately, studies that measure cortical neurophysiology during standing postural responses of people with a history of stroke remain untested. Nevertheless, studies on stroke highlight the importance of the cortex for selecting and shaping postural response synergies and also highlight needs for understanding the neural mechanisms of altered postural responses following stroke.
Table
Research on aging and cortical function during postural responses has largely been inferred through dual-task costs on the postural response under the assumption that a second task requires cortical resources and, therefore, any effects on postural responses reflect use of cortical resources during the response (Jacobs and Horak,
Recordings of cortical function during postural responses could provide key insight for identifying the mechanisms and circumstances of impairment, which could subsequently direct more optimized intervention. Unfortunately, only one study has attempted to compare EEG potentials evoked by perturbations of standing balance in young and older adults (Duckrow et al.,
In addition to the instability and falls associated with the impaired postural responses of people with PD, one of the more striking aspects is the lack of response modification based on contextual information about the upcoming perturbation's characteristics (Table
Because PD is often characterized as a disorder of diminished movement and cortical excitation during voluntary action, a contextually unmodified postural response might be predicted to associate with diminished preparatory potentials suggestive of a cortical incapacity to generate such potentials. Insights from EEG recordings of preparatory cortical function (contingent negative variation and event related desynchronization), however, demonstrate that people with PD fail to modulate their postural response by over-responding to small perturbations while concomitantly exhibiting increased desynchronization of upper beta (20–29 Hz) EEG signals prior to small perturbations. Further, larger desynchronization corresponds with less modulation of the postural response between small and large perturbation magnitudes (Smith et al.,
Given that preparatory cortical functions appear intact and over-responsive rather than incapacitated, these insights have significant ramifications for the potential to utilize behavioral and physical rehabilitation in order to train contextual response modulation. In addition, pharmacological or stimulation interventions would be directed differently for an over-responsive vs. under-responsive neurophysiologic condition. Therefore, this example in PD demonstrates the important value of recording cortical function during postural responses, because the neural mechanisms of a response may not be as expected based on behavioral inference alone.
Chronic pain due to musculoskeletal injury such as LBP can significantly alter the central neural control of postural coordination. Although all phases of a postural response can be altered with LBP, the more consistent and significant findings are an enhanced muscle co-activation prior to perturbations and strongly diminished late-phase trunk muscle responses with concomitant increases in distal muscle responses (Table
The examples above demonstrate that cortical neurophysiology during postural responses to extrinsic perturbations of standing balance is critical for individuals with postural impairments such as advanced aging, neurodegeneration, and chronic pain. In addition, the little available literature emphasizes how recordings of cortical neurophysiology during extrinsically induced postural responses can offer crucial insights into mechanisms of impaired balance that are not available or unexpected based on behavioral inference alone. Lastly, cortical neurophysiology is functionally relevant to the stability of postural responses and, perhaps, to clinical disability associated with the health condition.
Despite the importance of understanding the neurophysiologic mechanisms of impaired postural responses to extrinsic perturbations of standing balance, very little neurophysiologic recording beyond the muscle has been attempted during these responses. With technologies such as EEG, near infrared spectroscopy, single photon emission computed tomography, transcranial magnetic or direct-current stimulation, etc., and with improved abilities to overcome technical challenges, the opportunity for expansive research on the neurophysiology of extrinsically induced postural responses exists in order to compliment parallel work on voluntary postural control. For any population with disorders of balance and posture, more research is needed to evaluate multiple measures that reflect unique neurophysiologic systems of both preparatory and evoked neural activation. In addition, these recordings should be undertaken across multiple contexts that vary predictability, perturbation characteristics, dual tasking, etc. to more accurately understand how environmental circumstances affect the neural control of postural responses. In so doing, crucial insights are likely to emerge that could support more efficacious interventions and clinical outcomes for those with balance disorders.
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.