Human Electrocortical Dynamics While Stepping over Obstacles

Overview

Journal Sci Rep

Specialty Science

Date 2019 Mar 20

PMID 30886202

Citations 50

Authors

Andrew D Nordin

W David Hairston

Daniel P Ferris

Affiliations

Soon will be listed here.

Abstract

To better understand human brain dynamics during visually guided locomotion, we developed a method of removing motion artifacts from mobile electroencephalography (EEG) and studied human subjects walking and running over obstacles on a treadmill. We constructed a novel dual-layer EEG electrode system to isolate electrocortical signals, and then validated the system using an electrical head phantom and robotic motion platform. We collected data from young healthy subjects walking and running on a treadmill while they encountered unexpected obstacles to step over. Supplementary motor area and premotor cortex had spectral power increases within ~200 ms after object appearance in delta, theta, and alpha frequency bands (3-13 Hz). That activity was followed by similar posterior parietal cortex spectral power increase that decreased in lag time with increasing locomotion speed. The sequence of activation suggests that supplementary motor area and premotor cortex interrupted the gait cycle, while posterior parietal cortex tracked obstacle location for planning foot placement nearly two steps ahead of reaching the obstacle. Together, these results highlight advantages of adopting dual-layer mobile EEG, which should greatly facilitate the study of human brain dynamics in physically active real-world settings and tasks.

Citing Articles

The effects of acute exercise intensity on memory: Controlling for state-dependence.

Loprinzi P, Fuglaar L, Mangold R, Petty S, Jung M, Day L Mem Cognit. 2024; .

PMID: 39542975 DOI: 10.3758/s13421-024-01660-2.

Exploring Electrocortical Signatures of Gait Adaptation: Differential Neural Dynamics in Slow and Fast Gait Adapters.

Jacobsen N, Ferris D eNeuro. 2024; 11(7).

PMID: 38871456 PMC: 11242882. DOI: 10.1523/ENEURO.0515-23.2024.

Linking Dementia Pathology and Alteration in Brain Activation to Complex Daily Functional Decline During the Preclinical Dementia Stages: Protocol for a Prospective Observational Cohort Study.

De Sanctis P, Mahoney J, Wagner J, Blumen H, Mowrey W, Ayers E JMIR Res Protoc. 2024; 13:e56726.

PMID: 38842914 PMC: 11190628. DOI: 10.2196/56726.

Prefrontal cortical activity during uneven terrain walking in younger and older adults.

Hwang J, Liu C, Winesett S, Chatterjee S, Gruber 2nd A, Swanson C Front Aging Neurosci. 2024; 16:1389488.

PMID: 38765771 PMC: 11099210. DOI: 10.3389/fnagi.2024.1389488.

Mobile neuroimaging: What we have learned about the neural control of human walking, with an emphasis on EEG-based research.

Richer N, Bradford J, Ferris D Neurosci Biobehav Rev. 2024; 162:105718.

PMID: 38744350 PMC: 11813811. DOI: 10.1016/j.neubiorev.2024.105718.

References

Drew T, Andujar J, Lajoie K, Yakovenko S . Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res Rev. 2007; 57(1):199-211. DOI: 10.1016/j.brainresrev.2007.07.017. View

Duffy C, WURTZ R . Multiple temporal components of optic flow responses in MST neurons. Exp Brain Res. 1997; 114(3):472-82. DOI: 10.1007/pl00005656. View

Kline J, Huang H, Snyder K, Ferris D . Isolating gait-related movement artifacts in electroencephalography during human walking. J Neural Eng. 2015; 12(4):046022. PMC: 4946867. DOI: 10.1088/1741-2560/12/4/046022. View

Wagner J, Solis-Escalante T, Grieshofer P, Neuper C, Muller-Putz G, Scherer R . Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects. Neuroimage. 2012; 63(3):1203-11. DOI: 10.1016/j.neuroimage.2012.08.019. View

Jahn K, Wagner J, Deutschlander A, Kalla R, Hufner K, Stephan T . Human hippocampal activation during stance and locomotion: fMRI study on healthy, blind, and vestibular-loss subjects. Ann N Y Acad Sci. 2009; 1164:229-35. DOI: 10.1111/j.1749-6632.2009.03770.x. View

Haefeli J, Vogeli S, Michel J, Dietz V . Preparation and performance of obstacle steps: interaction between brain and spinal neuronal activity. Eur J Neurosci. 2010; 33(2):338-48. DOI: 10.1111/j.1460-9568.2010.07494.x. View

Siegel R, Read H . Analysis of optic flow in the monkey parietal area 7a. Cereb Cortex. 1997; 7(4):327-46. DOI: 10.1093/cercor/7.4.327. View

Makeig S, Westerfield M, Jung T, Enghoff S, Townsend J, Courchesne E . Dynamic brain sources of visual evoked responses. Science. 2002; 295(5555):690-4. DOI: 10.1126/science.1066168. View

Andujar J, Lajoie K, Drew T . A contribution of area 5 of the posterior parietal cortex to the planning of visually guided locomotion: limb-specific and limb-independent effects. J Neurophysiol. 2009; 103(2):986-1006. DOI: 10.1152/jn.00912.2009. View

10.

Schaafsma S, Duysens J . Neurons in the ventral intraparietal area of awake macaque monkey closely resemble neurons in the dorsal part of the medial superior temporal area in their responses to optic flow patterns. J Neurophysiol. 1996; 76(6):4056-68. DOI: 10.1152/jn.1996.76.6.4056. View

11.

Hamacher D, Herold F, Wiegel P, Hamacher D, Schega L . Brain activity during walking: A systematic review. Neurosci Biobehav Rev. 2015; 57:310-27. DOI: 10.1016/j.neubiorev.2015.08.002. View

12.

Gwin J, Ferris D . An EEG-based study of discrete isometric and isotonic human lower limb muscle contractions. J Neuroeng Rehabil. 2012; 9:35. PMC: 3476535. DOI: 10.1186/1743-0003-9-35. View

13.

Bradford J, Lukos J, Ferris D . Electrocortical activity distinguishes between uphill and level walking in humans. J Neurophysiol. 2015; 115(2):958-66. DOI: 10.1152/jn.00089.2015. View

14.

Marigold D, Drew T . Posterior parietal cortex estimates the relationship between object and body location during locomotion. Elife. 2017; 6. PMC: 5650472. DOI: 10.7554/eLife.28143. View

15.

Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T . Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage. 2004; 23(3):1020-6. DOI: 10.1016/j.neuroimage.2004.07.002. View

16.

Seeber M, Scherer R, Wagner J, Solis-Escalante T, Muller-Putz G . High and low gamma EEG oscillations in central sensorimotor areas are conversely modulated during the human gait cycle. Neuroimage. 2015; 112:318-326. DOI: 10.1016/j.neuroimage.2015.03.045. View

17.

Gordon J, Rankin J, Daley M . How do treadmill speed and terrain visibility influence neuromuscular control of guinea fowl locomotion?. J Exp Biol. 2015; 218(Pt 19):3010-22. PMC: 4631773. DOI: 10.1242/jeb.104646. View

18.

Patla A, Prentice S . The role of active forces and intersegmental dynamics in the control of limb trajectory over obstacles during locomotion in humans. Exp Brain Res. 1995; 106(3):499-504. DOI: 10.1007/BF00231074. View

19.

Drew T . Motor cortical cell discharge during voluntary gait modification. Brain Res. 1988; 457(1):181-7. DOI: 10.1016/0006-8993(88)90073-x. View

20.

Day B, Thompson P, Harding A, Marsden C . Influence of vision on upper limb reaching movements in patients with cerebellar ataxia. Brain. 1998; 121 ( Pt 2):357-72. DOI: 10.1093/brain/121.2.357. View