Movement Improves the Quality of Temporal Perception and Decision-Making

Abstract A critical aspect of behavior is that mobile organisms must be able to precisely determine where and when to move. A better understanding of the mechanisms underlying precise movement timing and action planning is therefore crucial to understanding how we interact with the world around us. Recent evidence suggests that our experience of time is directly and intrinsically computed within the motor system, consistent with the theory of embodied cognition. To investigate the role of the motor system, we tested human subjects (n = 40) on a novel task combining reaching and time estimation. In this task, subjects were required to move a robotic manipulandum to one of two physical locations to categorize a concurrently timed suprasecond. Critically, subjects were divided into two groups: one in which movement during the interval was unrestricted and one in which they were restricted from moving until the stimulus interval had elapsed. Our results revealed a higher degree of precision for subjects in the free-moving group. A further experiment (n = 14) verified that these findings were not due to proximity to the target, counting strategies, bias, or movement length. A final experiment (n = 10) replicated these findings using a within-subjects design, performing a time reproduction task, in which movement during encoding of the interval led to more precise performance. Our findings suggest that time estimation may be instantiated within the motor system as an ongoing readout of timing judgment and confidence.

[1]  G. Sandini,et al.  Motor Commands Induce Time Compression for Tactile Stimuli , 2013, The Journal of Neuroscience.

[2]  D. Wolpert,et al.  Changing your mind: a computational mechanism of vacillation , 2009, Nature.

[3]  Marcelo Gomes Mattar,et al.  de Bruijn cycles for neural decoding , 2011, NeuroImage.

[4]  Tomas Knapen,et al.  Interregional alpha-band synchrony supports temporal cross-modal integration , 2014, NeuroImage.

[5]  J. Kalaska,et al.  Comparison of variability of initial kinematics and endpoints of reaching movements , 1999, Experimental Brain Research.

[6]  Wilsaan M. Joiner,et al.  The decay of motor adaptation to novel movement dynamics reveals an asymmetry in the stability of motion state-dependent learning , 2017, PLoS Comput. Biol..

[7]  Ryota Kanai,et al.  Ready steady slow: action preparation slows the subjective passage of time , 2012, Proceedings of the Royal Society B: Biological Sciences.

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

[9]  D. Wolpert,et al.  Principles of sensorimotor learning , 2011, Nature Reviews Neuroscience.

[10]  Ramon Bartolo,et al.  The Context of Temporal Processing Is Represented in the Multidimensional Relationships between Timing Tasks , 2008, PloS one.

[11]  Alexandre Gramfort,et al.  The Strength of Alpha–Beta Oscillatory Coupling Predicts Motor Timing Precision , 2019, The Journal of Neuroscience.

[12]  R. Ivry,et al.  Moving Time: The Influence of Action on Duration Perception , 2014, Journal of experimental psychology. General.

[13]  D. Burr,et al.  Optimal Encoding of Interval Timing in Expert Percussionists , 2011, The Journal of Neuroscience.

[14]  G. Sandini,et al.  Active movement restores veridical event-timing after tactile adaptation. , 2012, Journal of neurophysiology.

[15]  Richard B Ivry,et al.  Temporal Control and Coordination: The Multiple Timer Model , 2002, Brain and Cognition.

[16]  M. Morrone,et al.  Perceived visual time depends on motor preparation and direction of hand movements , 2016, Scientific Reports.

[17]  Stephen M. Rao,et al.  “One-thousandone … one-thousandtwo …”: Chronometric counting violates the scalar property in interval timing , 2004, Psychonomic bulletin & review.

[18]  S. Nishida,et al.  Apparent Time Interval of Visual Stimuli Is Compressed during Fast Hand Movement , 2015, PloS one.

[19]  Gary C. Sing,et al.  Primitives for Motor Adaptation Reflect Correlated Neural Tuning to Position and Velocity , 2009, Neuron.

[20]  Tomohisa Asai,et al.  My action lasts longer: Potential link between subjective time and agency during voluntary action , 2017, Consciousness and Cognition.

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

[22]  R. Ivry,et al.  Time on Your Hands: Perceived Duration of Sensory Events Is Biased Toward Concurrent Actions , 2017, Journal of experimental psychology. General.

[23]  H. Mannila,et al.  Computing Discrete Fréchet Distance ∗ , 1994 .

[24]  M. García-Pérez,et al.  Does time ever fly or slow down? The difficult interpretation of psychophysical data on time perception , 2014, Front. Hum. Neurosci..

[25]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[26]  Masami Ishihara,et al.  Horizontal spatial representations of time: Evidence for the STEARC effect , 2008, Cortex.

[27]  H. Zelaznik,et al.  Correlations for timing consistency among tapping and drawing tasks: evidence against a single timing process for motor control. , 1999, Journal of experimental psychology. Human perception and performance.

[28]  Martin Wiener,et al.  An Intrinsic Role of Beta Oscillations in Memory for Time Estimation , 2018, Scientific Reports.

[29]  Satu Palva,et al.  The role of cortical beta oscillations in time estimation , 2016, Human brain mapping.

[30]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[31]  Michael S Landy,et al.  Motor control is decision-making , 2012, Current Opinion in Neurobiology.

[32]  Sylvain Baillet,et al.  Motor origin of temporal predictions in auditory attention , 2017, Proceedings of the National Academy of Sciences.

[33]  A. Haith,et al.  Independence of Movement Preparation and Movement Initiation , 2016, The Journal of Neuroscience.

[34]  Kielan Yarrow,et al.  How the motor system both encodes and influences our sense of time , 2016, Current Opinion in Behavioral Sciences.

[35]  Ellen Poliakoff,et al.  Good vibrations: Human interval timing in the vibrotactile modality , 2009, Quarterly journal of experimental psychology.

[36]  Md. Shoaibur Rahman,et al.  Selective Attention Gates the Interactive Crossmodal Coupling between Perceptual Systems , 2017, Current Biology.

[37]  Derek H. Arnold,et al.  Weighted Integration Suggests That Visual and Tactile Signals Provide Independent Estimates About Duration , 2017, Journal of experimental psychology. Human perception and performance.

[38]  R. VanRullen,et al.  Spontaneous EEG oscillations reveal periodic sampling of visual attention , 2010, Proceedings of the National Academy of Sciences.

[39]  Michael Schutz,et al.  “Moving to the beat” improves timing perception , 2013, Psychonomic Bulletin & Review.

[40]  Helmut Alt,et al.  Computing the Fréchet distance between two polygonal curves , 1995, Int. J. Comput. Geom. Appl..

[41]  Michael N. Shadlen,et al.  Temporal context calibrates interval timing , 2010, Nature Neuroscience.

[42]  Hugo Merchant,et al.  Linking Perception, Cognition, and Action: Psychophysical Observations and Neural Network Modelling , 2014, PloS one.

[43]  H. Coslett,et al.  Continuous Carryover of Temporal Context Dissociates Response Bias from Perceptual Influence for Duration , 2014, PloS one.

[44]  D. Wolpert,et al.  A common mechanism underlies changes of mind about decisions and confidence , 2015, eLife.

[45]  Martin Verner,et al.  Larger visual stimuli are perceived to last longer from time to time: The internal clock is not affected by nontemporal visual stimulus size. , 2015, Journal of vision.

[46]  Konrad Paul Kording,et al.  Relevance of error: what drives motor adaptation? , 2009, Journal of neurophysiology.

[47]  Ryota Kanai,et al.  Frequency tuning for temporal perception and prediction , 2016, Current Opinion in Behavioral Sciences.

[48]  Felix Wichmann,et al.  The psychometric function: II. Bootstrap-based confidence intervals and sampling , 2001, Perception & psychophysics.

[49]  J. Krakauer,et al.  Error correction, sensory prediction, and adaptation in motor control. , 2010, Annual review of neuroscience.

[50]  Ingo Fründ,et al.  Inference for psychometric functions in the presence of nonstationary behavior. , 2011, Journal of vision.

[51]  Anne-Claire Rattat,et al.  What is the best and easiest method of preventing counting in different temporal tasks? , 2012, Behavior research methods.

[52]  Luc H. Arnal,et al.  Delta-Beta Coupled Oscillations Underlie Temporal Prediction Accuracy. , 2015, Cerebral cortex.

[53]  H. Zelaznik,et al.  Dissociation of explicit and implicit timing in repetitive tapping and drawing movements. , 2002, Journal of experimental psychology. Human perception and performance.

[54]  Jörn Diedrichsen,et al.  Perceptual decisions are biased by the cost to act , 2017, eLife.

[55]  Karl M Newell,et al.  The movement speed-accuracy relation in space-time. , 2013, Human movement science.

[56]  Bingni W. Brunton,et al.  Rats and Humans Can Optimally Accumulate Evidence for Decision-Making , 2013, Science.

[57]  John W Krakauer,et al.  A motor planning stage represents the shape of upcoming movement trajectories. , 2016, Journal of neurophysiology.

[58]  Brandie M. Stewart,et al.  Rapid Automatic Motor Encoding of Competing Reach Options. , 2017, Cell reports.

[59]  C. Spence,et al.  Audiotactile interactions in temporal perception , 2011, Psychonomic bulletin & review.

[60]  R Plamondon,et al.  Speed/accuracy trade-offs in target-directed movements , 1997, Behavioral and Brain Sciences.