“He followed in his father’s footsteps, but his gait was somewhat erratic.” Nicolas Bentley
“Enthusiasm is the sparkle in your eyes, the swing in your gait.” Henry Ford
Introduction: There are no enjoyable aspects of Parkinson’s. The symptoms of Parkinson’s go from tolerable to bad and then to the worst. As the disorder progresses, a frequent event that occurs is termed freezing of gait, or FOG. And FOG aligns with the worst aspect of Parkinson’s. The video below illustrates FOG.
FOG can occur in any phase of Parkinson’s, but typically as one transitions to a more advanced stage, see Okuma and Yanagisawa [Ref 1], Amboni et al. [Ref 2], and Hallett [Ref3]. FOG occurs when the person-with-Parkinson’s (PwP) temporarily cannot move their feet, feeling as if they are glued to the floor. It often happens at doorways, during turns, while navigating narrow spaces, changing floor surfaces, walking in the dark, or under stress. For me, FOG occurs in small spaces, such as when walking/turning in a closet, stepping through a doorway, changing surfaces on the floor from carpet to wood, walking into a pitch-black, dark room, and simply turning. As always with Parkinson’s, everyone who experiences FOG is slightly different than another PwP in what obstacles influence their FOG.
The negative impact of FOG in PwP is clearly an increased risk of falls. Thus, FOG also contributes to the decrease in quality of life for PwP.
“Walk like it’s for sale and the rent is due tonight!” Miss J.
Mechanism Behind FOG:
(1) “Off-On” interface for carbidopa/levodopa– The occurrence of FOG begins with the difficulty of a PwP maintaining levels of levodopa; in other words, during the “off” phase of levodopa. In the initial phase of taking carbidopa/levodopa, one appears to experience a milder transition of levodopa from off to on and back to off. Unfortunately, as Parkinson’s disease progresses, there are fewer dopaminergic neurons available to take up levodopa, and the on-to-off transition seems to occur much faster. It is not the levodopa that has changed, it is our brain. Think of it this way: a brain full of dopaminergic neurons is like a tree full of leaves, providing shading to the house from the summer sun. As we transition from summer to the fall season, many leaves fall off the tree, allowing the sun to shine into the house. As with the levodopa issue, the sun has not changed; the tree has just shed its leaves (i.e., dopaminergic neurons).
Thus, the first clue to the cause of FOG is a disconnect between dopaminergic neurons and the motor unit . This also suggests that FOG occurs more frequently in the “off” phase in the body’s residual response to carbidopa/levodopa, see Okuma and Yanagisawa [Ref 1], Amboni et al. [Ref 2], and Hallett [Ref3].
(2) Gait and multi-tasking- Gait is a skilled movement and usually occurs automatically. In PwP, gait movement is not nearly as automatic and usually requires some cognitive capacity input. This suggests that FOG may occur more frequently when the PwP is multi-tasking, i.e., performing both gait function and some cognitive duty. If you are susceptible to FOG, keep walking from point A to point B as the sole task, and do not try to make it a walk complicated by some mental activity that detracts from the process of walking, see Zhang et al. [Ref 4] and Monaghan et al. [Ref 5].
(3) Reduction in cognition and executive function- Amboni et al. [Ref 2] reported that “on” state is linked to cognitive frontal lobe disorder (i.e., executive function). Their results suggest that the severity of FOG is associated with the severity of cognitive impairment. Scholl et al. [Ref 10] found that the more severe the loss of cognition results in an increase in FOG. These findings imply that as Parkinson’s advances in terms of disease severity, it causes gait abnormalities and changes in cognition that enhance the occurrence of FOG.
(4) Alterations in the basal ganglia and extrastriatal brain areas over time can promote FOG- In a study of >200 PwP, over a period of 12 years, Forsaa et al. [Ref 11] reported that as PwP aged, they developed FOG. At the start of the study, 27% of the study group had FOG, and by the end of the study, this had increased to 63%. These findings imply that FOG is common as PwP age and develop motor problems/complications.
(5) Task-based functional MRI measurements found links in the cognitive, motor, and limbic signatures in PwP with FOG- Ehgoetz Martens et al. [Ref 7] performed an interesting study using MRI measurements during a foot pedaling study compared to the results of the Freezing of Gait Questionnaire. I should acknowledge that the use and processing of many neural circuits are modified in Parkinson’s, and these changes occur with aging and the progression of the disease. The results of this study suggest that unique neural signature patterns are associated with FOG.
(6) Visual complications alter gait, which can promote FOG– It should be obvious how vital sight is to gait and balance, Stuart et al [Ref 6]. However, vision is a complex sensory system that uses multiple structures and levels of information for processing. Vision functions in many areas, including visual acuity, contrast sensitivity, dynamic visual acuity, motion perception, and optic flow. Unfortunately, visual problems are common in advanced aging, and this definitely includes individuals with Parkinson’s. Age-related vision issues affect quality of life, mobility, and increase the risk of falls. Vision issues definitely influence gait, which could contribute to FOG.
(7 ) Poor sleep quality is linked to FOG: Two studies, Tang et al. [Ref 9] and de Almeida et al. [Ref 8], report on the impact of sleep on FOG. Their findings indicate that poor sleep quality increases the occurrence of FOG, and this relationship is unrelated to the stage of disease. A summary of FOG information suggests that motor (e.g., turning), cognitive (e.g., dual-tasking), and affective (e.g., anxiety) scenarios can all contribute to FOG. This suggests that dampening of the thalamus and pedunculopontine (PPN) is involved in FOG. These neural circuits (thalamus and PPN) are also involved in the wake-sleep cycle and rapid eye movement (REM) sleep. Thus, these studies show that poor sleep quality contributes to FOG and worsens cognitive impairment, anxiety, and mobility. Therefore, correcting or improving sleep issues in PwP could help reduce the occurrence of FOG.
Summary- Numerous aspects of the brain appear to contribute to FOG in Parkinson’s. Clearly, the description of published work strongly suggests that neural network defects in motor function, cognition, anxiety, limbic, vision, and sleep can all contribute to FOG. In many PwP, FOG may occur more frequently as they age and require increased amounts of carbidopa/levodopa, which is likely due to changes in the “off-on” cycle. FOG does occur in the “on” phase, but is more likely to happen during the “off” phase of levodopa. Collectively, FOG results from substantial changes in the PwP’s brain. FOG is likely not preventable, especially as the PwP progresses to the advanced stage.
“Gentleness in the gait is what simplicity is in the dress. Violent gestures or quick movements inspire involuntary disrespect.” Honore de Balzac
But hope is not totally lost: The following section outlines steps to reduce the risk of FOG occurring, as well as tips on managing FOG when it does happen. Understanding how these dysfunctional neural networks interact could lead to the development of new treatments for FOG. In the meantime, individuals with Parkinson’s should consult a physical therapist for strategies to manage and counter the detrimental effects of FOG.
“Cats have intercepted my foot steps at the ankle for so long that my gait, both at home and on tour, has been compared to that of a man wading through low surf.” Roy Blount, Jr.
Ways to Reduce Freezing of Gait (FOG):
Almost every organization focused on Parkinson’s will have a handout available to help a PwP deal with FOG. As mentioned above, there are many different factors that can trigger the frozen step, and numerous dysfunctional neural pathways promote FOG. Thus, I encourage you to explore multiple sources and see which process, suggestion, or aid can best help you if FOG develops or occurs in your life. Here is a sampling of some material with proven ways to handle FOG when it happens:
Freezing and PD (click here);
6 Ways to Reduce Freezing of Gait (click here);
Freezing of Gait in Parkinson’s disease (click here).
“Wise men read very sharply all of your private history in your look and gait and behavior.” Ralph Waldo Emerson
A Few Things I Do to Deal with FOG: When I began experiencing these freezing moments, I scheduled a time with one of my Physical Therapists. I left our session with some simple suggestions. These are the ones that are locked in my memory (they work for me, and I encourage you to read the above handouts and see your PT to figure out what can work for you):
(1) When FOG occurs, stop whatever I am doing, gather my thoughts, and breathe in and out a few times.
(2) Importantly, and for me a big one, do not get angry; this has happened, it is part of your Parkinson’s, and a calm mind and response will get you through the process.
(3) Be very aware that you do not want to fall, so think and do the below;
(4) Using a slightly larger step than usual, move the left leg forward while swinging the right arm as you begin to walk. Make it a controlled walk going straight, focus on walking deliberately but not fast (stay upright as you walk);
(5) Another thing that might help is to move your arms back and forth without walking, trying to stretch a little.
(6) Do not multitask, for instance, I may be carrying a cup of coffee and an iced electrolyte drink when an early morning event might happen. I put down one drink and made the trip twice between the start and finish spots. Or if it is dark, before I make those trips, I turn on the lights first.
(7) Upon approaching an archway/door frame, or needing to make a turn, stop! Re-establish calmness, imagine the task first, and then focus on turning or migrating through the doorway, staying focused. And don’t get angry.
(8) Wearing socks (make sure they are NOT slippery) or shoes helps me during the event, as sliding or slippery surfaces are complex in the moment of FOG;
(9) Do not try to walk through these frozen feet; it is imperative to stop, assess, and walk forward/backward as outlined above. The FOG will melt away with the planned movement.
(10) Dosing of carbidopa-levodopa needs to be optimized by you and your Neurologist. It is essential to ensure the “on-off” interface is optimized, to stay “on” for more extended periods than being “off”. An obvious big issue for anyone with FOG is what happens while you are asleep, and the time from the last evening dose to the first dose the next morning? When you wake up, you are “off” or “on,” and what is the possibility of FOG occurring?
“Let me tell you what I look like: pale face, long hair, and a tiny start of a paunch. In addition, an awkward gait, and a cigar in the mouth and a pen in pocket or hand.” Albert Einstein
Two Examples of FOG (one difficult experience and one hopeful experience):
•The difficult experience- We were recently at Pensacola Beach in Florida for a few days of beach time following my annual family reunion. I had been on the beach, doing very little besides enjoying the sunshine and the waves coming into the sparkling white sandy beach. The path from the beach to the covered parking spot for the car, below the resort, was about 200-300 yards from our beach chairs, umbrella, and small cooler. Walking through the sand first, carrying a chair and a wrapped-up umbrella, and then a wooden ramp of steps and a walkway, I set out to walk. I knew as I walked that I was overdue for the next dose of Crexont (an extended-release version of carbidopa-levodopa). Towards the end of the wooden-framed walkway approaching the resort, it took a turn of maybe 25-30 degrees. And the sun shining through the wood slats was totally different, and this immediately brought on the FOG. I stopped, Susan looked back at me and said, “Just stay there.” A couple behind me asked if I needed help; I said, “Thanks, but no thanks, I just need to stay still and focus for a few seconds.” By then, Susan had reached the car, dropped her chair, and returned to take my chair and beach umbrella. I slowly completed the walk to the car and then took the elevator into the resort. Lesson learned (for me)- When it happens, the off-rate of Crexont is no slower than the traditional carbidopa-levodopa rate (but Crexont does have a longer on-time). So, for me, off is off, and if I am tired, anxious, or stressed, it may put me in a situation where FOG could happen.
•The hopeful experience- Preparing for this blog post had me reading a lot about FOG. At the same time, I have been working hard to improve my sleep habits and trying to enhance the quality of my sleep, while also increasing my nightly sleep time. Recently, I was able to sleep two out of three nights for 8-9 consecutive hours (where my usual sleep time is 4-5 hours). I know from experience that if I am getting only 3-4 hours of sleep, I am prone to waking up with FOG. In both of these longer sleep nights, I woke up alert and was walking totally normally with no evidence of FOG. I should also mention that when I did wake up in these two instances, it had been ~12 hours since taking my previous evening dose of Crexont (carbidopa/levodopa). Lesson learned (for me)- Sleep matters. Sleep plays a crucial role in managing the daily symptoms of Parkinson’s. Of course, the problematic issue is maintaining both the quality and time of sleep I can achieve each night. But as described throughout this blog post, FOG really sucks big-time. And I am going to keep trying anything I can to prevent FOG from being a frequent participant in my life.
“Look, the world’s comforter, with weary gait,
His day’s hot task hath ended in the west:
The owl, night’s herald, shrieks-’tis very late;
The sheep are gone to fold, birds to their nest;
And coal-black clouds, that shadow heaven’s light,
Do summon us to part, and bid good night.” William Shakespeare
References:
1. Okuma, Y.; Yanagisawa, N. The clinical spectrum of freezing of gait in Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society 2008, 23, S426-S430.
2. Amboni, M.; Cozzolino, A.; Longo, K.; Picillo, M.; Barone, P. Freezing of gait and executive functions in patients with Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society 2008, 23, 395-400.
3. Hallett, M. The intrinsic and extrinsic aspects of freezing of gait. Movement disorders: official journal of the Movement Disorder Society 2008, 23, S439-S443.
4. Zhang, F.; Shi, J.; Duan, Y.; Cheng, J.; Li, H.; Xuan, T.; Lv, Y.; Wang, P.; Li, H. Clinical features and related factors of freezing of gait in patients with Parkinson’s disease. Brain and behavior 2021, 11, e2359.
5. Monaghan, A.S.; Gordon, E.; Graham, L.; Hughes, E.; Peterson, D.S.; Morris, R. Cognition and freezing of gait in Parkinson’s disease: A systematic review and meta-analysis. Neurosci Biobehav Rev 2023, 147, 105068, doi:10.1016/j.neubiorev.2023.105068.
6. Stuart, S.; Lord, S.; Hill, E.; Rochester, L. Gait in Parkinson’s disease: A visuo-cognitive challenge. Neurosci Biobehav Rev 2016, 62, 76-88, doi:10.1016/j.neubiorev.2016.01.002.
7. Ehgoetz Martens, K.A.; Hall, J.M.; Georgiades, M.J.; Gilat, M.; Walton, C.C.; Matar, E.; Lewis, S.J.; Shine, J.M. The functional network signature of heterogeneity in freezing of gait. Brain 2018, 141, 1145-1160.
8. de Almeida, F.O.; Ugrinowitsch, C.; Brito, L.C.; Milliato, A.; Marquesini, R.; Moreira-Neto, A.; Barbosa, E.R.; Horak, F.B.; Mancini, M.; Silva-Batista, C. Poor sleep quality is associated with cognitive, mobility, and anxiety disability that underlie freezing of gait in Parkinson’s disease. Gait & posture 2021, 85, 157-163.
9. Tang, X.; Yu, L.; Yang, J.; Guo, W.; Liu, Y.; Xu, Y.; Wang, X. Association of sleep disturbance and freezing of gait in Parkinson disease: prevention/delay implications. Journal of Clinical Sleep Medicine 2021, 17, 779-789.
10. Scholl, J.L.; Espinoza, A.I.; Rai, W.; Leedom, M.; Baugh, L.A.; Berg-Poppe, P.; Singh, A. Relationships between freezing of gait severity and cognitive deficits in Parkinson’s disease. Brain Sciences 2021, 11, 1496.
1. Okuma, Y.; Yanagisawa, N. The clinical spectrum of freezing of gait in Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society 2008, 23, S426-S430.
2. Amboni, M.; Cozzolino, A.; Longo, K.; Picillo, M.; Barone, P. Freezing of gait and executive functions in patients with Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society 2008, 23, 395-400.
3. Hallett, M. The intrinsic and extrinsic aspects of freezing of gait. Movement disorders: official journal of the Movement Disorder Society 2008, 23, S439-S443.
4. Zhang, F.; Shi, J.; Duan, Y.; Cheng, J.; Li, H.; Xuan, T.; Lv, Y.; Wang, P.; Li, H. Clinical features and related factors of freezing of gait in patients with Parkinson’s disease. Brain and behavior 2021, 11, e2359.
5. Monaghan, A.S.; Gordon, E.; Graham, L.; Hughes, E.; Peterson, D.S.; Morris, R. Cognition and freezing of gait in Parkinson’s disease: A systematic review and meta-analysis. Neurosci Biobehav Rev 2023, 147, 105068, doi:10.1016/j.neubiorev.2023.105068.
6. Stuart, S.; Lord, S.; Hill, E.; Rochester, L. Gait in Parkinson’s disease: A visuo-cognitive challenge. Neurosci Biobehav Rev 2016, 62, 76-88, doi:10.1016/j.neubiorev.2016.01.002.
7. Ehgoetz Martens, K.A.; Hall, J.M.; Georgiades, M.J.; Gilat, M.; Walton, C.C.; Matar, E.; Lewis, S.J.; Shine, J.M. The functional network signature of heterogeneity in freezing of gait. Brain 2018, 141, 1145-1160.
8. de Almeida, F.O.; Ugrinowitsch, C.; Brito, L.C.; Milliato, A.; Marquesini, R.; Moreira-Neto, A.; Barbosa, E.R.; Horak, F.B.; Mancini, M.; Silva-Batista, C. Poor sleep quality is associated with cognitive, mobility, and anxiety disability that underlie freezing of gait in Parkinson’s disease. Gait & posture 2021, 85, 157-163.
9. Tang, X.; Yu, L.; Yang, J.; Guo, W.; Liu, Y.; Xu, Y.; Wang, X. Association of sleep disturbance and freezing of gait in Parkinson disease: prevention/delay implications. Journal of Clinical Sleep Medicine 2021, 17, 779-789.
10. Scholl, J.L.; Espinoza, A.I.; Rai, W.; Leedom, M.; Baugh, L.A.; Berg-Poppe, P.; Singh, A. Relationships between freezing of gait severity and cognitive deficits in Parkinson’s disease. Brain Sciences 2021, 11, 1496.
11. Forsaa, E.; Larsen, J.; Wentzel-Larsen, T.; Alves, G. A 12-year population-based study of freezing of gait in Parkinson’s disease. Parkinsonism & related disorders 2015, 21, 254-258.
Journey with Parkinson's 