The Neuroscience of Pathologic Gait and Posture

Gait and posture are two of the most complicated processes in the human body that require a tremendous amount of neural resources. Whether dealing with Parkinson’s, multiple sclerosis, stroke or even a simple orthopaedic injury, the brain has the ability to recognize, reorganize and compensate in response to environmental, physical, and neural changes (Nanhoe-Mahabier et al., 2011). The importance and application of understanding the underlying mechanisms of walking and posture goes well beyond neurorehabilitation and opens a window into the phenomenology of consciousness. Though in order to keep it short and relevant, this post focuses on the neural bases and pathological causes of gait disturbance and potential corrective measures.

If you have ever sprained your ankle or seen someone else walking after a mild ankle injury  you must have noticed a change in their gait.  Transverse loading and weight shifting change dramatically, exaggerated weight shifting and loading to the unaffected side is almost always an automatic process that occurs instantly after the injury.  In stroke, and other movement disorders same gait changes are observed but due to different causes (Consult table-1 in the reference section).

One thing movement disorders have in common is the fact that if we disregard mechanical abnormalities for the sake of simplification, all other forms of gait disturbances involve the rewiring of neural networks, whether it is due to cerebellar infarcts that causes ataxia, bradykinetic patterns in dopamine dependent basal ganglia (BG) malfunction in Parkinson’s or hemiplegia in stroke, the compensatory mechanisms arise few hours , days or months after the onset. In return, neural activity patterns and locations of those activities change from the deeper structures of the brain such as areas highly involved in procedural memory in the midbrain region and motor area (MA) and the supplementary motor area (SMA) all the way to the frontal areas and the executive system such as the dorsolateral prefrontal cortex (DLPFC) (Takakusaki, 2017) , as if a previously effortless movement that could be achieved without a deliberate stepwise cognitive process, now could be achieved only haphazardly and by shifting a tremendous amount effort and attention in order to carry out such tasks.  Just think about the amount of cognitive resources needed for the simple act of walking:  peripheral nerves, spinal cord, proprioceptors, sensory and motor pathways, vision, vestibular system, comparators in the brain, and many other processes that are required for a balanced, coordinated and efficient act of walking (Tattersall et al., 2014).

Figure 1:  Brain regions involved in walking. Picture Credit: (“The walking brain | Atlas of Science,” n.d.)

 

I hope you are convinced that walking is nothing but an amazing cognitive task that in the absence of pathology somehow we manage to perform it almost effortlessly and automatically. Holism vs localism aside, It would be a disservice to the field of neuroscience not to ask the question of nature vs. nurture! Is walking a hardwired and innate phenomenon or is it learned?  how come we can walk for hours and multitask without thinking extensively about how to adjust our dorsiflexions with the terrain we are walking on? Why do babies not walk out of the womb and how come aging and dementia affect walking to the point of immobility? let us go through an example:

Right MCA stroke with Craniectomy

As you can see in this video, a patient with a history of a large right middle cerebral artery infarct and decompressive craniectomy has shown an amazing improvement both in ambulation and posture. If you pay attention to the MRI at the beginning of the video, and the images below you see extensive damage to the frontal and temporal areas of the right hemisphere with encephalomalacia. Normally if you have not seen the patient prior to looking at this MRI you would be baffled to learn this patient is not wheelchair bound, and capable of walking without any help. Despite gait disturbances and postural instability this case teaches us valuable lessons in regards to neural rewiring and/or compensatory strategies developed by cortical regions previously not involved in the process of walking and posture. The compensatory strategies are often the ones  that have the lowest energy requirement and cognitive load, hence the unnatural gait in stroke survivors. This patient can walk and display much better movements if she was walking up the stairs while holding on to the railing on the side, but the fear and uncertainty caused by lack of proprioception and hemianesthesia do not allow the adequate evaluation of the affected side by the brain which leads to further postural instability and compensatory mechanisms. Although the cerebellar system is intact in this case, this patient still presents patterns of imbalance during ambulation, simply due to lack of harmonious muscular activation that was originally achieved by the collaboration between the sensory, pre motor and motor networks in conjunction with thalamic and basal ganglia pathways. Let us look through a couple of important cerebral networks that may play a role in decoupling of effortless automatic movements versus effortful deliberate movements. I want you to think about a guitar player on the stage  who plays the instrument, and sings accompanied with rhythmic body movements. How is it possible that a novice guitar learner requires an extensive amount of focus and as the learner excels in the mastery of the instrument, multitasking becomes easier and playing complex melodies will be achieved without extensive effort. how about a basketball player who can dribble the ball  without even thinking about it almost as if the ball is an extension of his body and the act of dribbling is as simple as walking?

 

The Default Mode Network 

This network is inversely correlated with attention.  let us think of an example: you are driving home after a long ED shift and when you arrive home, you have no idea how you got home so fast, you might not even be able to recall the details of the trip home. The default mode network is also correlated with the memory and simulation systems, it compares events happened in the past and creating an imaginary model of the possible future events. It is also involved in learning, multiple resting state fMRI studies have shown higher activities in the default mode network regions (as shown below) rather than other cortical areas when comparing novice learners vs masters (Labriffe et al., 2017). Somehow mastery level is synonymous with lower cortical activities and higher activities in subcortical and deep structures (Yuan, Blumen, Verghese, & Holtzer, 2015).  For instance when you learn how to ride a bike after a few days and weeks of practice you can almost effortlessly look around pedal and enjoy the sceneries.  This can be thought of as the difference between the rookie and the pro athletes, rookies try too hard, burn joules of calories to perform a same task that pros could do with their eyes closed. it is simply because the expert or the pro saves their executive and higher level cognitive areas to pay attention to details other than fundamentals.

Figure -2: The default mode network

 

Another Example: Internal Capsule Stroke and Abnormal Gait Patterns 

Internal capsule is just an example of one of the subtypes of stroke that impedes movement. In this type of subcortical stroke the internal capsule which is a highway of motor and sensory fibres above the level of basal ganglia becomes hypoperfused  leading to apoptosis causing sensory and motor weaknesses in the contralateral side. Patients usually present with hyperflexia, sensory and/or motor loss, Babinski, Hoffman’s, clonus and spasticity (Bansil et al., 2012).  Also, due to the location of such lesions, truncal and postural instability (not ataxia) present due to miscommunication between the brainstem, and higher cortical regions. Depending on the extent of the damage these patient might or might not be able to walk, but the interesting thing about their recovery is the fact that they develop multiple compensatory strategies to transfer or walk. They are capable of doing better and have a closer to natural pattern of walking and movement only when they constantly remind themselves the ABCs of walking. And this is where the default mode network and other areas involved in effortless movement fall short, causing an overload in higher cortical regions such frontal and prefrontal regions (see figure 2). Since this is a resource intensive use of the neural networks, patients with such pathologies often have difficulties performing multiple tasks. One way to test such hypothesis is by adding multiple external stimuli and just observe their gait patterns. Anyone who has ever seen a stroke patient would know that step-wise approach, a flat terrain, and a quite environment will drastically improve performance of these patients, but the moment these patients go back in the society outside the rehab facilities, their ability to move and ambulate declines dramatically.

Figure -3: The internal capsule: motor and sensory involvement. 

 

Philosophical, Neuroscientific and Clinical Repercussion of Multisystem Arrangement of the Brain

Locomotion in biological entities is an evolutionary act of moving from one place to another in order to maintain life, whether it is to run away from danger, finding food, or maintenance of homeostasis, we, alongside other species have been able to automatized the act of movement as a background neural process while engaging in higher power and more costly neural activities. Although multiple netwroks in our brains function simultaneously to optimize sensation and perception in order to generate the appropriate behaviour, but the existence of a two tiered system (the default mode network vs. cortical networks) is an amazing neuro-architectural feature that cannot be taken for granted.  Let us think about the following words: reflex, instinct, habit, and reason, Think about these words from a neuroscientific perspective, and here I am going to quote Charles Darwin:

Now, think about this in a “default network vs higher cortical system ” sense! It is amazing how Charles Darwin understood this very fundamental architectural feature of most nervous systems capable of higher computational capabilities, and we are still having a hard time implementing such knowledge into our day to day clinical practice as a common sense.  Let us go back to the words:

Reflex: An action or movement not controlled by a conscious thought.

Instinct: An innate, typically fixed pattern of behaviour in animals in response to certain stimuli.

Habit: A predictable behaviour that originally was not innate but acquired, and is semi-automatic in nature, conscious volition can change or extinct the behaviour.

Reason: whether you call it reason, computation, insight or analytical power, it is indicative of higher power thinking, analysis, morality, goal directed behaviour, learning, etc.

Holism aside, the above words are representatives of neural networks and systems in the brain. Let us think about the processes of learning a new task. Reason is the portal of entry, this is where sensation and perception join together, but nothing will be coded until deemed meaningful by the cortical comparators. Now that the nervous system takes the perceived stimulus worthy of absorption, habit kicks in, this is where rehearsal occurs to the point that the nervous system makes a habit out of  the targeted task. It is habit that makes the execution of a task much more cost effective, sometimes to the point that they become  genetic codes, and favourable for the fitness of the species, and eventually get passed on to the next generations. If you are asking how? then you should ask the following question and google the answer! how does a spider know how to web even if it is raised in solitude?

Although we are all aware of the developmental basis of locomotion and posture, and their instinctive basis, but I have observed something quite astonishing while caring for stroke patients. It seems as if though these patients have an open window for reprogramming instinctive behaviours (movement related). To me,  when a stroke damages parts of the homunculus, initially involved in for example the dorsiflexion of the foot, the procedural memory for that specific movement cannot be accessed, most of stroke victims develop a unique pattern of movement and despite further improvements and recovery they continue with the initially coded movement patterns ( learned in the first few days and weeks after stroke). Somehow the movement pattern that is learned during the few first weeks will become the cost effective, and innate way of movement for these patients. Unfortunately, although low neural cost of such patterns rearranges the involved networks, but poor body mechanics and physical deterioration (i.e. osteoarthritis of malaligned and spastic joints ) accompanied with the natural process of aging, will eventually take a toll on these patients, isolating them from the society and affecting their life span.

 

Better Treatment Plan, Better Recovery

Recovery after stroke continues as long as individuals have a high level of involvement in the society, whether through volunteerism, day programs or even joining the work force. Therefore, the acute phase of stroke (first few weeks) is critical in order to create the appropriate movement habits. Just like bad parenting, the medical team and rehab staff with poor knowledge, and lack of motivation can negatively affect patients’ recovery outcomes. Also one size fit all treatment plans whether physical, psychological and/or pharmaceutical only works to manage, and not to improve outcomes.

 

 

 

Appendix:

 

                             Figure 4- Physiology of gait (Fasano & Bloem, 2013)

 

 

 

 

Table 1: Type of gait abnormalities.

 

References:

1- Fasano, A., & Bloem, B. R. (2013). Gait disorders. Continuum (Minneapolis, Minn.), 19(5 Movement Disorders), 1344–1382. https://doi.org/10.1212/01.CON.0000436159.33447.69
Gait Abnormalities | Stanford Medicine 25 | Stanford Medicine. (n.d.). Retrieved June 2, 2017, from https://stanfordmedicine25.stanford.edu/the25/gait.html
2- Giladi, N., Horak, F. B., & Hausdorff, J. M. (2013). Classification of gait disturbances: distinguishing between continuous and episodic changes. Movement Disorders : Official Journal of the Movement Disorder Society, 28(11). https://doi.org/10.1002/mds.25672
3- Kaski, D., & Bronstein, A. M. (2014). Treatments for Neurological Gait and Balance Disturbance: The Use of Noninvasive Electrical Brain Stimulation. Advances in Neuroscience, 2014. https://doi.org/10.1155/2014/573862
4- Labriffe, M., Annweiler, C., Amirova, L. E., Gauquelin-Koch, G., Ter Minassian, A., Leiber, L.-M., … Dinomais, M. (2017). Brain Activity during Mental Imagery of Gait Versus Gait-Like Plantar Stimulation: A Novel Combined Functional MRI Paradigm to Better Understand Cerebral Gait Control. Frontiers in Human Neuroscience, 11. https://doi.org/10.3389/fnhum.2017.00106
5- Nanhoe-Mahabier, W., Snijders, A. H., Delval, A., Weerdesteyn, V., Duysens, J., Overeem, S., & Bloem, B. R. (2011). Walking patterns in Parkinson’s disease with and without freezing of gait. Neuroscience, 182, 217–224. https://doi.org/10.1016/j.neuroscience.2011.02.061
6- Study of gait as a biomarker for cognitive decline – Institute of Neuroscience – Newcastle University. (n.d.). Retrieved June 2, 2017, from http://www.ncl.ac.uk/ion/research/neurodegenerative/ncpdproj3/
7- Takakusaki, K. (2017). Functional Neuroanatomy for Posture and Gait Control. Journal of Movement Disorders, Journal of Movement Disorders, 10(1), 1–17. https://doi.org/2017.10.1.1
8- Tattersall, T. L., Stratton, P. G., Coyne, T. J., Cook, R., Silberstein, P., Silburn, P. A., … Sah, P. (2014). Imagined gait modulates neuronal network dynamics in the human pedunculopontine nucleus. Nature Neuroscience, 17(3), 449–454. https://doi.org/10.1038/nn.3642
9- The walking brain | Atlas of Science. (n.d.). Retrieved June 2, 2017, from https://atlasofscience.org/the-walking-brain/
10- Verghese, J., Ambrose, A. F., Lipton, R. B., & Wang, C. (2010). Neurological Gait Abnormalities And Risk Of Falls In Older Adults. Journal of Neurology, 257(3), 392–398. https://doi.org/10.1007/s00415-009-5332-y
11- Yuan, J., Blumen, H. M., Verghese, J., & Holtzer, R. (2015). Functional Connectivity Associated With Gait Velocity During Walking and Walking-While-Talking in Aging: A Resting-State fMRI Study. Human Brain Mapping, 36(4), 1484–1493. https://doi.org/10.1002/hbm.22717

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