Walking entrains unique oscillations in performance on a visual detection task

Walking is among our most frequent and natural of voluntary behaviours, yet the consequences of locomotion upon perceptual and cognitive function remain largely unknown. Recent work has highlighted that although walking feels smooth and continuous, critical phases exist within each step-cycle for the successful coordination of perceptual and motor function. Here, we tested whether these phasic demands impact upon visual perception, by assessing performance in a visual detection task during natural unencumbered walking. We finely sampled visual performance over the stride cycle as participants walked along a smooth linear path at a comfortable speed in a wireless virtual reality environment. At the group-level, accuracy, reaction times, and response likelihood showed strong oscillations, modulating at approximately 2 cycles-per-stride (∼2 Hz) with a marked phase of optimal performance aligned with the swing phase of each step. At the participant level, Bayesian inference of population prevalence revealed highly prevalent oscillations that clustered in two idiosyncratic frequency ranges (2 or 4 cycles per stride), with a strong phase alignment across participants.

[1]  Frans A. J. Verstraten,et al.  Peripersonal tracking accuracy is limited by the speed and phase of locomotion , 2023, bioRxiv.

[2]  Liyu Cao,et al.  Human visual processing during walking: Dissociable pre- and post-stimulus influences , 2022, NeuroImage.

[3]  Robin A. A. Ince,et al.  Within-participant statistics for cognitive science , 2022, Trends in Cognitive Sciences.

[4]  Liyu Cao,et al.  Differential effects of walking across visual cortical processing stages , 2022, Cortex.

[5]  D. Heck,et al.  Respiratory rhythms of the predictive mind. , 2021, Psychological review.

[6]  Barry Giesbrecht,et al.  Tracking the Contents of Spatial Working Memory during an Acute Bout of Aerobic Exercise , 2021, Journal of Cognitive Neuroscience.

[7]  Helge Hillnhütter Stimulating urban walking environments – Can we measure the effect? , 2021, Environment and Planning B: Urban Analytics and City Science.

[8]  Daniel S. Kluger,et al.  Respiration aligns perception with neural excitability , 2021, bioRxiv.

[9]  Liyu Cao,et al.  Overground Walking Decreases Alpha Activity and Entrains Eye Movements in Humans , 2020, Frontiers in Human Neuroscience.

[10]  Matthew C Smear,et al.  Movement-Related Signals in Sensory Areas: Roles in Natural Behavior , 2020, Trends in Neurosciences.

[11]  Daniel S. Kluger,et al.  Respiration modulates oscillatory neural network activity at rest , 2020, bioRxiv.

[12]  Jennifer L. Campos,et al.  Iterative Spatial Updating During Forward Linear Walking Revealed Using a Continuous Pointing Task , 2020, Journal of motor behavior.

[13]  Sten Grillner,et al.  Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion. , 2020, Physiological reviews.

[14]  Liyu Cao,et al.  Walking enhances peripheral visual processing in humans , 2019, PLoS biology.

[15]  Anthony J. Ries,et al.  Effect of locomotor demands on cognitive processing , 2019, Scientific Reports.

[16]  C. Tallon-Baudry,et al.  Visceral Signals Shape Brain Dynamics and Cognition , 2019, Trends in Cognitive Sciences.

[17]  M. Morrone,et al.  Behavioural oscillations in visual orientation discrimination reveal distinct modulation rates for both sensitivity and response bias , 2019, Scientific Reports.

[18]  S. Kastner,et al.  A Rhythmic Theory of Attention , 2019, Trends in Cognitive Sciences.

[19]  W. Klimesch The frequency architecture of brain and brain body oscillations: an analysis , 2018, The European journal of neuroscience.

[20]  R. VanRullen Attention Cycles , 2018, Neuron.

[21]  M. Pinsk,et al.  A Dynamic Interplay within the Frontoparietal Network Underlies Rhythmic Spatial Attention , 2018, Neuron.

[22]  Mary M. Hayhoe,et al.  Gaze and the Control of Foot Placement When Walking in Natural Terrain , 2018, Current Biology.

[23]  David C. Burr,et al.  Auditory Sensitivity and Decision Criteria Oscillate at Different Frequencies Separately for the Two Ears , 2017, Current Biology.

[24]  Jessica A. Cardin,et al.  Sensation during Active Behaviors , 2017, The Journal of Neuroscience.

[25]  D. Heck,et al.  Rhythms of the body, rhythms of the brain: Respiration, neural oscillations, and embodied cognition , 2017, Consciousness and Cognition.

[26]  Sean L. Barton,et al.  The critical phase for visual control of human walking over complex terrain , 2017, Proceedings of the National Academy of Sciences.

[27]  E. Maris,et al.  Theta oscillations locked to intended actions rhythmically modulate perception , 2017, eLife.

[28]  Stefan Glasauer,et al.  Quantification of Head Movement Predictability and Implications for Suppression of Vestibular Input during Locomotion , 2017, Front. Comput. Neurosci..

[29]  John T. Serences,et al.  Acute Exercise Modulates Feature-selective Responses in Human Cortex , 2017, Journal of Cognitive Neuroscience.

[30]  Robert Kozma,et al.  Breathing as a Fundamental Rhythm of Brain Function , 2017, Frontiers in neural circuits.

[31]  R. VanRullen Perceptual Cycles , 2016, Trends in Cognitive Sciences.

[32]  Andreas Wutz,et al.  Temporal Integration Windows in Neural Processing and Perception Aligned to Saccadic Eye Movements , 2016, Current Biology.

[33]  M. Carandini,et al.  Vision and Locomotion Shape the Interactions between Neuron Types in Mouse Visual Cortex , 2016, Neuron.

[34]  M. Morrone,et al.  Rhythmic modulation of visual contrast discrimination triggered by action , 2016, Proceedings of the Royal Society B: Biological Sciences.

[35]  Alessandro Sale,et al.  A cycling lane for brain rewiring , 2015, Current Biology.

[36]  G. Sandini,et al.  Rhythmic Oscillations of Visual Contrast Sensitivity Synchronized with Action , 2015, The Journal of Neuroscience.

[37]  Kyuichi Niizeki,et al.  Cardiolocomotor phase synchronization during rhythmic exercise , 2014 .

[38]  C. Tallon-Baudry,et al.  Spontaneous fluctuations in neural responses to heartbeats predict visual detection , 2014, Nature Neuroscience.

[39]  Martin A. Giese,et al.  Kinematics of the Coordination of Pointing during Locomotion , 2013, PloS one.

[40]  P. Golshani,et al.  Cellular mechanisms of brain-state-dependent gain modulation in visual cortex , 2013, Nature Neuroscience.

[41]  B. Fajen,et al.  Humans exploit the biomechanics of bipedal gait during visually guided walking over complex terrain , 2013, Proceedings of the Royal Society B: Biological Sciences.

[42]  Romeo Chua,et al.  Muscle-specific modulation of vestibular reflexes with increased locomotor velocity and cadence. , 2013, Journal of neurophysiology.

[43]  H. Critchley,et al.  Visceral Influences on Brain and Behavior , 2013, Neuron.

[44]  Georg B. Keller,et al.  Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse , 2012, Neuron.

[45]  J. Gross,et al.  Sounds Reset Rhythms of Visual Cortex and Corresponding Human Visual Perception , 2012, Current Biology.

[46]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[47]  Patrick Cavanagh,et al.  The blinking spotlight of attention , 2007, Proceedings of the National Academy of Sciences.

[48]  Denis Cousineau,et al.  Confidence intervals in within-subject designs: A simpler solution to Loftus and Masson's method , 2005 .

[49]  J. T. Inglis,et al.  When is vestibular information important during walking? , 2004, Journal of neurophysiology.

[50]  A. Kuo,et al.  Comparison of kinematic and kinetic methods for computing the vertical motion of the body center of mass during walking. , 2004, Human movement science.

[51]  Cynthia A. Brewer,et al.  ColorBrewer.org: An Online Tool for Selecting Colour Schemes for Maps , 2003 .

[52]  B. Cohen,et al.  The Human Vestibulo‐Ocular Reflex during Linear Locomotion , 2001, Annals of the New York Academy of Sciences.

[53]  R. Carpenter,et al.  The neural control of looking , 2000, Current Biology.

[54]  F. Lacquaniti,et al.  Motor Patterns in Walking. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[55]  B. Cohen,et al.  Effects of walking velocity on vertical head and body movements during locomotion , 1999, Experimental Brain Research.

[56]  R. Banzett,et al.  Mechanical Links Between Locomotion and Breathing: Can You Breathe With Your Legs? , 1997 .

[57]  K Niizeki,et al.  Cardiac, respiratory, and locomotor coordination during walking in humans. , 1996, Folia primatologica; international journal of primatology.

[58]  P. Bernasconi,et al.  Analysis of co‐ordination between breathing and exercise rhythms in man. , 1993, The Journal of physiology.

[59]  K Niizeki,et al.  Interaction among cardiac, respiratory, and locomotor rhythms during cardiolocomotor synchronization. , 1993, Journal of applied physiology.

[60]  A. Berthoz,et al.  Head stabilization during various locomotor tasks in humans , 1990, Experimental Brain Research.

[61]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[62]  D. Bramble,et al.  Running and breathing in mammals. , 1983, Science.

[63]  G. K. Noorden Movements of the Eyes , 1978 .

[64]  P. MacNeilage Characterization of Natural Head Movements in Animals and Humans , 2020 .

[65]  J. Bloomberg,et al.  Identifying head-trunk and lower limb contributions to gaze stabilization during locomotion. , 2002, Journal of vestibular research : equilibrium & orientation.

[66]  D K C Macdonald Spontaneous fluctuations , 1949 .