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Effects of Movement-Based and Cognitive Priming on Brain Function

Katie Fabian

 


Background

Clinical research is something I knew I wanted to experience, especially given the phenomenal access and resources we have here at UNC. Therefore, I chose to participate in the research elective offered in the fall of 2019, working alongside Dr. Mike Lewek, PT, PhD, Dr. Jessica Cassidy PT, DPT, PhD, and Hannah Ryan, SPT. Dr. Lewek and Dr. Cassidy had planned an interesting collaborative project based in their combined expertise in rehabilitation after stroke, especially as it relates to gait, and neurological changes as observed by EEG. Together, we devised and completed a pilot study of the impacts of clinically feasible modes of priming on brain activity and connectivity.

I was personally drawn to this project due to my growing interest in rehabilitation of adults after a stroke. Through clinical experiences in hospitals, in-patient rehabilitation, an outpatient Neurological Integrated Clinical Experience, and interaction with individuals in the community, I have seen the need for efficient and effective rehabilitation across all stages following a stroke. To our patients, the most debilitating aspect of their stroke is the loss of independence, a loss often tied to deficits in walking. Therefore, this opportunity to research a treatment which could improve the efficiency of motor learning and gait training after stroke was too great to pass up.

 


Statement of Need

The prevalence of stroke and stroke survivorship are currently both increasing, resulting in stroke being one of the leading causes of long-term disability.1 Furthermore, currently 65-75% of stroke survivors have ongoing rehabilitation needs, for which access can be limited due to factors such as accessibility, cost, or geographical proximity.2,3 With reports that as many as 80% of stroke survivors experience difficulties with walking after stroke,4 and deficits persisting past 6 months in 25 – 30% of survivors, motor learning, especially related to gait, is an important intervention in rehabilitation after stroke.4,5 Current literature suggests that the ability of individuals to learn motor tasks after a stroke may be impaired due to a loss of neuroplasticity or imbalances in interhemispheric activity.6,7 These underlying changes to the brain may modulate progress in interventions that require motor learning or re-learning such as walking tasks.6

In the field of neurorehabilitation, the idea of “priming” is gaining interest as it may be able to facilitate improvements in these underlying changes to the brain.6,7 The basis of priming is that an exposure to a stimulus before a treatment intervention then changes the outcome of that treatment.7 Commonly studied examples of these stimuli are stimulation such as transcranial magnetic stimulation (TMS)8,9 or pharmacological agents such as cortisol or norepinephrine.10,11 Although both have shown to be effective in altering cortical excitability that is important for improved motor learning, neither of these are feasible clinical interventions for physical therapists.8–11 Therefore, priming interventions that are low cost, have minimal contraindications, or need little equipment or training should be researched as these are more clinically feasible.7 Our study builds on a small body of research regarding two “clinic ready” modes of priming. Cognitive stimuli such as motor imagery or action observation, and movement-based stimuli such as aerobic exercise are the two employed in this study.7,12 There is limited research on the efficacy of these modes of priming to influence motor learning in healthy individuals13,14 and those after stroke,15,16 but most available literature focuses on upper extremity tasks rather than gait. However, preliminary evidence indicates efficacy of priming in upper extremity tasks may not generalize to lower extremity tasks.17,18 Therefore, our study is nuanced in its aim to provide foundational information about two clinically feasible modes of priming as they relate to gait and locomotor learning.

Additionally, while priming is currently thought to affect motor learning and rehabilitation outcomes through induction of neuroplastic changes, the underlying neural mechanisms remain unclear.7 Consequently, this study will use electroencephalography (EEG) recordings to further understand changes in brain activation patterns that occur after different types of priming by tracking changes in electrical potentials generated in areas of the brain known to be involved with movement and gait. This understanding can help to inform not only future studies, but also may elucidate these underlying neural mechanisms of changes in receptivity to motor training.

 


Products

We started the writing process by creating an abstract which was submitted and accepted to the Human Movement Science Research Symposium at UNC. Although the symposium was canceled due to COVID-19, we created a presentation of our research and findings to present to the Cassidy Plasticity Lab group in a zoom meeting. A manuscript was written to share our findings, and will be submitted to peer-reviewed journals in the future for publication.

Priming Project Abstract

Priming Project Presentation

Priming Project Manuscript

Lastly, to address health literacy and facilitate understanding of possible future study participants, we created a handout that explains what priming is and our current understanding of its role in rehabilitation. Ideally this handout will be used in future work involving patient populations to assist in the explanation of the importance of our research as it relates to their recovery after stroke.

Priming Project Handout

 


Abstract

Introduction: Priming involves exposure to a stimulus in order to elicit a behavior change related to motor learning. Priming may involve neurostimulation, pharmacology, exercise, and mental imagery. The purpose of priming is to potentiate the effects of a subsequent activity. Past work demonstrated enhanced motor learning with the addition of a bout of priming delivered prior to a motor-learning activity. However, limited work has investigated the effects of priming on brain function.

Purpose: To determine the effects of priming on brain function using non-invasive electroencephalography (EEG). This study focused on two modes of priming: aerobic exercise (movement-based) and action observation (cognitive-based).

Methods: Healthy, right-handed individuals (≥18 years) completed baseline testing consisting of a behavioral battery and a three-minute resting-state EEG recording. Participants were randomized to receive either a five-minute movement- or cognitive-based priming intervention before crossing-over after one week to receive the remaining priming intervention. During these visits, participants completed a three-minute resting-state EEG recording before and immediately after priming. Movement-based priming consisted of walking on a treadmill while maintaining an established target heart rate range. Cognitive priming involved watching a video of individuals walking on a treadmill. Brain function was assessed by computing measures of EEG power and coherence (connectivity) across a predefined motor network in the high beta (20-30 Hz) frequency range. Changes in EEG power and coherence following priming were determined with two-sided paired t-tests.

Results: A total of 18 individuals participated with 17 completing all study visits. Data from 9 individuals (7 females) aged 24±2.8 years was included in the results. A significant increase in high beta coherence between electrodes overlying left primary motor cortex and supplementary motor area (t=3.08, p=0.018) was observed following aerobic priming. Action observation priming did not elicit changes in brain function.

Conclusion: Results show that aerobic exercise increases brain connectivity in a motor relevant circuit in healthy adults. Heightened connectivity following aerobic priming may have important implications related to subsequent motor learning and, in a neurorehabilitation setting, motor re-learning.

 


Self-Reflection

I am very proud of the work Hannah and I have put into this project, and am pleased with the end result. I am most proud of the manuscript itself, as I was less comfortable with academic writing. After many edits and discussions, am now more confident. I feel I have also gained important understanding of the research process, from the writing and submission to the Institutional Review Board (IRB), to the research and writing of a final manuscript. Although proficiency in academic-style writing is something I will continue to work on throughout my professional career, I am pleased with the growth I have seen in my abilities through this project.

My knowledge and skills relating to EEG data collection and processing are another area of significant growth for me. At the onset, I was unfamiliar with this research tool, but now feel competent not only in my use of EEG and decision-making during data processing, but also confident in explaining why we chose specifically to use this tool in our study, and what additional insight it can offer. Initially, we viewed the immense amount of EEG data to process as a potential barrier to progress in this project, but looking back I am very thankful for the learning opportunity this presented. Hannah and I were able to be trained in the evaluation and processing of EEG data, a skill set I had not been expecting to gain, but one that certainly helped us in the creation of the manuscript and presentation of our results. This situation taught me great lessons about not only attention to detail and analysis of data, but also the importance of teamwork and collaboration within a research team. I enjoyed the opportunity to learn not only from committee members, but also from other researchers and peers.

Overall, I am very proud of the work Hannah and I have done, my growth in knowledge and proficiency, and the outcome of our products. This has been a powerful learning experience and I am thankful for all aspects.

 


Evaluation

Through weekly meetings and frequent editing of the products associated with this Capstone project, Hannah and I received feedback from committee members starting with the process of data collection in the fall and through the writing process this spring. Multiple training sessions led by Dr. Jessica Cassidy, PT, DPT, PhD helped us to improve efficacy and quality of data collection through proficiency with use of EEG equipment. During this time, Dr. Mike Lewek, PT, PhD, used weekly meetings to evaluate progress and give guidance in problem solving in areas such as participant recruitment.

Dr. Jessica Cassidy also offered frequent feedback through the processing of the EEG data and writing of the manuscript. At the completion of each section of the manuscript, we would send it to her, and then incorporate her feedback through a series of edits until we created our final products. We also sent all final products to all committee members, and incorporated their feedback into the products to improve word choice and clarity.

We submitted an abstract to the Human Movement Science Research Symposium at UNC which was reviewed and accepted. Although this symposium was unable to take place this year due to regulations following COVID-19, Hannah and I presented our findings to Dr. Cassidy’s lab where we received questions and feedback from the group. Lastly, we are planning on having our manuscript published, so we will also receive feedback in the form of peer-reviews after it is sent in for publication.

 


Acknowledgments

Dr. Jessica Cassidy, PT, DPT, PhD – Thank you so much for your continued support, guidance, and availability (even while on maternity leave!) through data collection, processing, and the writing process. I have learned so much from you through this whole process, and am beyond thankful for the time and dedication to our project. Your feedback, insight, and quick problem-solving has been pivotal through this whole process, and we could not have done this without you. Truly, thank you for all you have done!

Dr. Mike Lewek, PT, PhD – Thank you so much for your continued support and guidance throughout this research process and last three years. Your dedication to your work and students has not gone unnoticed, and is greatly appreciated. Thank you for your availability, guidance, and willingness to talk-through all aspects of this research project with us, as well as your feedback and insight on our work. I am so very appreciative for all you have done!

Calvin Wang, PT – Thank you for serving on our Capstone Committee and providing Hannah and I with timely feedback on our products and manuscript. Your insight as a clinician provided us with very valuable feedback.

Hannah Ryan, SPT – Hannah, I cannot thank you enough for the work and time you have put into this project. You have been the perfect research partner, full of insight, good questions, and experience. I am so thankful for your hard work, problem-solving abilities, and partnership as we completed all steps of this project! This would not have been the same without you!

Cassidy Plasticity Lab Research assistants – To Jasper Mark, Jingles Jeangilles, Ramis Chowdhury, Hrishika Muthukrishnan, and Eric Zheng, I cannot thank you enough. Our project would not have been successful without the countless hours data processing undertaken by you all, and for that we are endlessly grateful.

Sara Galante, SPT – Thank you so much for your hard work filming and creating the videos used in our research intervention. You undertook a rather tedious task and completed it beautifully. Thank you so much for your role in making everything run so smoothly!

To our classmates – Thank you all for being so supportive of our project! Thank you to all who volunteered, participated, and supported us through this process, we could not have done it (or the past 3 years of school) without your support and encouragement. Thank you all, you are so appreciated.

 


References:

  1. Billinger SA, Arena R, Bernhardt J, et al. Physical activity and exercise recommendations for stroke survivors: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2014;45(8):2532-2553. doi:10.1161/STR.0000000000000022.
  2. National Institute of Neurological Disorders and Stroke. Post-Stroke Rehabilitation Fact Sheet. National Institute of Health (NIH) 2020. Available at: https://www.ninds.nih.gov/Disorders/Patient-Caregiver-Education/Fact-Sheets/Post-Stroke-Rehabilitation-Fact-Sheet. Accessed April 16, 2020.
  3. Appleby E, Gill ST, Hayes LK, Walker TL, Walsh M, Kumar S. Effectiveness of telerehabilitation in the management of adults with stroke: A systematic review. PLoS One 2019;14(11):e0225150. doi:10.1371/journal.pone.0225150.
  4. Li S, Francisco GE, Zhou P. Post-stroke Hemiplegic Gait: New Perspective and Insights. Front. Physiol. 2018;9:1021. doi:10.3389/fphys.2018.01021.
  5. Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics–2012 update: a report from the American Heart Association. Circulation 2012;125(1):e2-e220. doi:10.1161/CIR.0b013e31823ac046.
  6. Li S. Spasticity, Motor Recovery, and Neural Plasticity after Stroke. Front. Neurol. 2017;8:120. doi:10.3389/fneur.2017.00120.
  7. Stoykov ME, Madhavan S. Motor priming in neurorehabilitation. J Neurol Phys Ther 2015;39(1):33-42. doi:10.1097/NPT.0000000000000065.
  8. Cassidy JM, Chu H, Anderson DC, et al. A Comparison of Primed Low-frequency Repetitive Transcranial Magnetic Stimulation Treatments in Chronic Stroke. Brain Stimulat. 2015;8(6):1074-1084. doi:10.1016/j.brs.2015.06.007.
  9. Kwon TG, Park E, Kang C, Chang WH, Kim Y-H. The effects of combined repetitive transcranial magnetic stimulation and transcranial direct current stimulation on motor function in patients with stroke. Restor Neurol Neurosci 2016;34(6):915-923. doi:10.3233/RNN-160654.
  10. Milani P, Piu P, Popa T, et al. Cortisol-induced effects on human cortical excitability. Brain Stimulat. 2010;3(3):131-139. doi:10.1016/j.brs.2009.07.004.
  11. Ziemann U, Tam A, Bütefisch C, Cohen* LG. Dual modulating effects of amphetamine on neuronal excitability and stimulation-induced plasticity in human motor cortex. Clin. Neurophysiol. 2002;113(8):1308-1315. doi:10.1016/S1388-2457(02)00171-2.
  12. Stoykov ME, Corcos DM, Madhavan S. Movement-Based Priming: Clinical Applications and Neural Mechanisms. J Mot Behav2017;49(1):88-97. doi:10.1080/00222895.2016.1250716.
  13. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A single bout of moderate aerobic exercise improves motor skill acquisition. PLoS One2015;10(10):e0141393. doi:10.1371/journal.pone.0141393.
  14. Gonzalez-Rosa JJ, Natali F, Tettamanti A, et al. Action observation and motor imagery in performance of complex movements: evidence from EEG and kinematics analysis. Behav. Brain Res. 2015;281:290-300. doi:10.1016/j.bbr.2014.12.016.
  15. Valkenborghs SR, Visser MM, Dunn A, et al. AExaCTT – Aerobic Exercise and Consecutive Task-specific Training for the upper limb after stroke: Protocol for a randomised controlled pilot study. Contemp. Clin. Trials Commun. 2017;7:179-185. doi:10.1016/j.conctc.2017.07.009.
  16. Kuk E-J, Kim J-M, Oh D-W, Hwang H-J. Effects of action observation therapy on hand dexterity and EEG-based cortical activation patterns in patients with post-stroke hemiparesis. Top Stroke Rehabil 2016;23(5):318-325. doi:10.1080/10749357.2016.1157972.
  17. Patel J, Qiu Q, Yarossi M, et al. Exploring the impact of visual and movement based priming on a motor intervention in the acute phase post-stroke in persons with severe hemiparesis of the upper extremity. Disabil. Rehabil. 2017;39(15):1515-1523. doi:10.1080/09638288.2016.1226419.
  18. Charalambous CC, Alcantara CC, French MA, et al. A single exercise bout and locomotor learning after stroke: physiological, behavioural, and computational outcomes. J. Physiol. (Lond.) 2018;596(10):1999-2016. doi:10.1113/JP275881.

Featured Image Credit: Kurzweil

4 Responses to “Effects of Movement-Based and Cognitive Priming on Brain Function”

  1. kcfabian

    Sara,

    Thank you for your continued excitement for our project! I am so very thankful for your role in making the videos (which were flawless by the way) and I love that it helped motivate you in your own capstone! Thank you for being such a supportive classmate, you are quite a gem!

    Best,

    Katie

    Reply
  2. kcfabian

    Debbie,

    Thank you so much for your kind words and encouragement! It was truly such a fun and great learning experience for me! Both the completion of the data collection and turning it into a manuscript taught me a lot about the research process. We are also very excited and hopeful for the future publishing of our manuscript as well as the continued research that will be done as a progression to what we started!

    Thank you!

    Katie

    Reply
  3. Sara Galante

    Katie,
    It’s great to see the end result of your research! I know how hard you and Hannah have worked to make this project a reality and I am incredibly impressed with the manuscript, presentation, and handout. I’m sorry the research symposium was canceled but I hope that you will submit for another opportunity to present these findings so I can come listen! The contributions of you and Hannah under Dr.Lewek and Dr.Cassidy’s guidance are sure to be invaluable both to the profession and to UNC. I’m glad the videos helped so much because I had fun doing them! Working on your project even gave me confidence to pursue the filming and editing on my own capstone project. Amazing job to both of you and I’m excited to see where both this research and you two are headed in your careers!
    Sara

    Reply
  4. Debbie Thorpe

    Katie
    Wow! You and Hannah did a tremendous amount of work for this project! Congratulations on the abstract acceptance for HMSC Day. Even though you did not present it, you developed a wonderful ppt to present as an in-service for clinicians. I can’t wait to see the manuscript in publication! You patient flyer is also top quality. You both should be very proud of your accomplishements.
    Best Wishes…

    Reply

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