Natural rhythms of periodic temporal attention

That attention is a fundamentally rhythmic process has recently received abundant empirical evidence. The essence of temporal attention, however, is to flexibly focus in time. Whether this function is constrained by an underlying rhythmic neural mechanism is unknown. In six interrelated experiments, we behaviourally quantify the sampling capacities of periodic temporal attention during auditory or visual perception. We reveal the presence of limited attentional capacities, with an optimal sampling rate of ~1.4 Hz in audition and ~0.7 Hz in vision. Investigating the motor contribution to temporal attention, we show that it scales with motor rhythmic precision, maximal at ~1.7 Hz. Critically, motor modulation is beneficial to auditory but detrimental to visual temporal attention. These results are captured by a computational model of coupled oscillators, that reveals the underlying structural constraints governing the temporal alignment between motor and attention fluctuations. That attention is a rhythmic process has received abundant evidence. Here, the authors reveal the natural sampling rate of auditory and visual periodic temporal attention. Both are antagonistically modulated by overt motor activity, a result generalised in a dynamical model of coupled oscillators.

[1]  Ralph Barnes,et al.  Expectancy, Attention, and Time , 2000, Cognitive Psychology.

[2]  Karen Canfell,et al.  Cervical Abnormalities Are More Common among Indigenous than Other Australian Women: A Retrospective Record-Linkage Study, 2000–2011 , 2016, PloS one.

[3]  Aniruddh D. Patel,et al.  Temporal modulations in speech and music , 2017, Neuroscience & Biobehavioral Reviews.

[4]  D. Liberman,et al.  [Time perception]. , 1955, Revista de psicoanalisis.

[5]  C. Buss,et al.  Children's Brain Development Benefits from Longer Gestation , 2011, Front. Psychology.

[6]  Rufin VanRullen,et al.  The Psychophysics of Brain Rhythms , 2011, Front. Psychology.

[7]  Assaf Breska,et al.  Automatic Bias of Temporal Expectations following Temporally Regular Input Independently of High-level Temporal Expectation , 2014, Journal of Cognitive Neuroscience.

[8]  C. Drake,et al.  The development of rhythmic attending in auditory sequences: attunement, referent period, focal attending , 2000, Cognition.

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

[10]  Bert De Smedt,et al.  Visual Number Beats Abstract Numerical Magnitude: Format-dependent Representation of Arabic Digits and Dot Patterns in Human Parietal Cortex , 2015, Journal of Cognitive Neuroscience.

[11]  Quanli Wang,et al.  meaRtools: An R package for the analysis of neuronal networks recorded on microelectrode arrays , 2018, bioRxiv.

[12]  Keith Johnson,et al.  Encoding of Articulatory Kinematic Trajectories in Human Speech Sensorimotor Cortex , 2018, Neuron.

[13]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[14]  G. Pellizzer,et al.  The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity , 2019, Front. Integr. Neurosci..

[15]  Paul Fraisse,et al.  II. - Rythmes auditifs et rythmes visuels , 1948 .

[16]  David Poeppel,et al.  Rhythmicity and cross-modal temporal cues facilitate detection , 2014, Neuropsychologia.

[17]  S. Kotz,et al.  Cortico-striatal circuits and the timing of action and perception , 2016, Current Opinion in Behavioral Sciences.

[18]  E. Vaucher,et al.  Activation of the mouse primary visual cortex by medial prefrontal subregion stimulation is not mediated by cholinergic basalo-cortical projections , 2015, Front. Syst. Neurosci..

[19]  Viktor K. Jirsa,et al.  Phase-lags in large scale brain synchronization: Methodological considerations and in-silico analysis , 2018, PLoS Comput. Biol..

[20]  Elyse Sussman,et al.  Auditory Target Detection Is Affected by Implicit Temporal and Spatial Expectations , 2011, Journal of Cognitive Neuroscience.

[21]  S. Haegens,et al.  Rhythmic facilitation of sensory processing: A critical review , 2017, Neuroscience & Biobehavioral Reviews.

[22]  C. Schroeder,et al.  Multi-Scale Entrainment of Coupled Neuronal Oscillations in Primary Auditory Cortex , 2015, Front. Hum. Neurosci..

[23]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[24]  D. Burr,et al.  Auditory dominance over vision in the perception of interval duration , 2009, Experimental Brain Research.

[25]  Huan Luo,et al.  Behavioral Oscillations in Attention: Rhythmic α Pulses Mediated through θ Band , 2014, The Journal of Neuroscience.

[26]  Nathaniel S. Miller,et al.  The time of our lives: life span development of timing and event tracking. , 2006, Journal of experimental psychology. General.

[27]  Nicolas Farrugia,et al.  BAASTA: Battery for the Assessment of Auditory Sensorimotor and Timing Abilities , 2016, Behavior Research Methods.

[28]  L. Boroditsky,et al.  Time in the mind: Using space to think about time , 2008, Cognition.

[29]  M. Jones,et al.  Temporal Aspects of Stimulus-Driven Attending in Dynamic Arrays , 2002, Psychological science.

[30]  Luc H. Arnal,et al.  Entrained delta oscillations reflect the subjective tracking of time , 2017, Communicative & integrative biology.

[31]  Charles E. Schroeder,et al.  Motor contributions to the temporal precision of auditory attention , 2014, Nature Communications.

[32]  Karl J. Friston,et al.  Not All Predictions Are Equal: “What” and “When” Predictions Modulate Activity in Auditory Cortex through Different Mechanisms , 2018, The Journal of Neuroscience.

[33]  Li Wang,et al.  Corrigendum: The Serum Profile of Hypercytokinemia Factors Identified in H7N9-Infected Patients can Predict Fatal Outcomes , 2016, Scientific reports.

[34]  Hamish G MacDougall,et al.  Marching to the beat of the same drummer: the spontaneous tempo of human locomotion. , 2005, Journal of applied physiology.

[35]  ON THE FACTORS OF THE MENTAL TEMPO , 1956 .

[36]  Jennifer H. Wisecaver,et al.  Drivers of genetic diversity in secondary metabolic gene clusters within a fungal species , 2017, bioRxiv.

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

[38]  Massimiliano Di Luca,et al.  Optimal Perceived Timing: Integrating Sensory Information with Dynamically Updated Expectations , 2016, Scientific Reports.

[39]  David Poeppel,et al.  Neural Entrainment to the Beat: The “Missing-Pulse” Phenomenon , 2017, The Journal of Neuroscience.

[40]  Seul Lee,et al.  Temporal Dynamics of Visual Attention Allocation , 2019, Scientific Reports.

[41]  K. Lange Brain correlates of early auditory processing are attenuated by expectations for time and pitch , 2009, Brain and Cognition.

[42]  B. K. Wiederhold,et al.  Kozlik, J., Neumann, R. & Kunde, W. (in press). ABC versus QWERTZ: Interference from mismatching sequences of letters in the alphabet and on the keyboard. Journal of Experimental Psychology: Human Perception and Performance. , 2012 .

[43]  D. Moelants Preferred tempo reconsidered. , 2002 .

[44]  Anna C. Nobre,et al.  Synergistic Effect of Combined Temporal and Spatial Expectations on Visual Attention , 2005, The Journal of Neuroscience.

[45]  Thomas M. Hall,et al.  A Common Structure Underlies Low-Frequency Cortical Dynamics in Movement, Sleep, and Sedation , 2014, Neuron.

[46]  Timothy D Griffiths,et al.  Temporal predictions based on a gradual change in tempo. , 2012, The Journal of the Acoustical Society of America.

[47]  Phillip Wolff,et al.  Causal reasoning with forces , 2015, Front. Hum. Neurosci..

[48]  T. Womelsdorf,et al.  Long-Range Attention Networks: Circuit Motifs Underlying Endogenously Controlled Stimulus Selection , 2015, Trends in Neurosciences.

[49]  Michael J. Spivey,et al.  Compatibility of motion facilitates visuomotor synchronization. , 2010, Journal of experimental psychology. Human perception and performance.

[50]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[51]  E. Large,et al.  Neural Networks for Beat Perception in Musical Rhythm , 2015, Front. Syst. Neurosci..

[52]  M. Wachowiak All in a Sniff: Olfaction as a Model for Active Sensing , 2011, Neuron.

[53]  P. Montague,et al.  Ready…Go: Amplitude of the fMRI Signal Encodes Expectation of Cue Arrival Time , 2009, PLoS biology.

[54]  Lisa D. Sanders,et al.  Local and global auditory processing: Behavioral and ERP evidence , 2007, Neuropsychologia.

[55]  Luc H. Arnal,et al.  Temporal Prediction in lieu of Periodic Stimulation , 2016, The Journal of Neuroscience.

[56]  E. Large,et al.  The dynamics of attending: How people track time-varying events. , 1999 .

[57]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[58]  Luc H. Arnal,et al.  Proactive Sensing of Periodic and Aperiodic Auditory Patterns , 2018, Trends in Cognitive Sciences.

[59]  N. Hatsopoulos,et al.  Fast and Slow Oscillations in Human Primary Motor Cortex Predict Oncoming Behaviorally Relevant Cues , 2010, Neuron.

[60]  Charles E. Schroeder,et al.  The Role of Neuronal Oscillations in Visual Active Sensing , 2019, Front. Integr. Neurosci..

[61]  C. Schroeder,et al.  Tuning of the Human Neocortex to the Temporal Dynamics of Attended Events , 2011, The Journal of Neuroscience.

[62]  Aniruddh D. Patel,et al.  UC Office of the President Recent Work Title Synchronization to auditory and visual rhythms in hearing and deaf individuals Permalink , 2014 .

[63]  P. Schwartzkroin,et al.  Neural mechanisms. , 1994, Science.

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

[65]  M. Siegel,et al.  A framework for local cortical oscillation patterns , 2011, Trends in Cognitive Sciences.

[66]  M. Grube,et al.  A Unified Model of Time Perception Accounts for Duration-Based and Beat-Based Timing Mechanisms , 2011, Front. Integr. Neurosci..

[67]  E. Wagenmakers,et al.  A default Bayesian hypothesis test for correlations and partial correlations , 2012, Psychonomic bulletin & review.

[68]  Matthew T. Kaufman,et al.  A neural network that finds a naturalistic solution for the production of muscle activity , 2015, Nature Neuroscience.

[69]  Charles E. Schroeder,et al.  Prominence of delta oscillatory rhythms in the motor cortex and their relevance for auditory and speech perception , 2019, Neuroscience & Biobehavioral Reviews.

[70]  M. Cecchini,et al.  Ultrastructural Characterization of the Lower Motor System in a Mouse Model of Krabbe Disease , 2016, Scientific Reports.

[71]  W. Meck,et al.  Neuroanatomical and Neurochemical Substrates of Timing , 2011, Neuropsychopharmacology.

[72]  M. R. Jones,et al.  Time, our lost dimension: toward a new theory of perception, attention, and memory. , 1976, Psychological review.

[73]  Aldenor G. Santos,et al.  Occurrence of the potent mutagens 2- nitrobenzanthrone and 3-nitrobenzanthrone in fine airborne particles , 2019, Scientific Reports.

[74]  J. Gross,et al.  Individual Human Brain Areas Can Be Identified from Their Characteristic Spectral Activation Fingerprints , 2016, PLoS biology.

[75]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[76]  B. Hangya,et al.  Phase Entrainment of Human Delta Oscillations Can Mediate the Effects of Expectation on Reaction Speed , 2010, The Journal of Neuroscience.

[77]  Knight Dunlap,et al.  Reaction to rhythmic stimuli with attempt to synchronize. , 1910 .

[78]  David Cai,et al.  Effects of Firing Variability on Network Structures with Spike-Timing-Dependent Plasticity , 2018, Front. Comput. Neurosci..

[79]  John J. Foxe,et al.  Auditory facilitation of visual-target detection persists regardless of retinal eccentricity and despite wide audiovisual misalignments , 2011, Experimental Brain Research.

[80]  Y. Ejima,et al.  Does Temporal Expectation Driven by Rhythmic Cues Differ From That Driven by Symbolic Cues Across the Millisecond and Second Range? , 2019, Perception.

[81]  Jan W. H. Schnupp,et al.  Temporal Processing in Audition: Insights from Music , 2017, Neuroscience.

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

[83]  Aniruddh D. Patel,et al.  The influence of metricality and modality on synchronization with a beat , 2005, Experimental Brain Research.

[84]  K. Kwack,et al.  Upregulation of the NLRC4 inflammasome contributes to poor prognosis in glioma patients , 2019, Scientific Reports.

[85]  Timothy D. Griffiths,et al.  Distinct Neural Substrates of Duration-Based and Beat-Based Auditory Timing , 2011, The Journal of Neuroscience.

[86]  A. Vallesi,et al.  Neural dissociation of automatic and controlled temporal preparation by transcranial magnetic stimulation , 2014, Neuropsychologia.

[87]  Craig G. Richter,et al.  Feature-Based Attention Samples Stimuli Rhythmically , 2019, Current Biology.

[88]  P. Dayan,et al.  Pharmacological Fingerprints of Contextual Uncertainty , 2016, PLoS biology.

[89]  Ramesh Balasubramaniam,et al.  Sensorimotor Synchronization With Auditory and Visual Modalities: Behavioral and Neural Differences , 2018, Front. Comput. Neurosci..

[90]  Petr Janata,et al.  Mapping the Dynamic Allocation of Temporal Attention in Musical Patterns , 2018, Journal of experimental psychology. Human perception and performance.

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

[92]  Yoshiki Kuramoto,et al.  Self-entrainment of a population of coupled non-linear oscillators , 1975 .

[93]  N. Hatsopoulos,et al.  Sensing with the Motor Cortex , 2011, Neuron.

[94]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[95]  Peter Lakatos,et al.  Dynamics of Active Sensing and perceptual selection , 2010, Current Opinion in Neurobiology.

[96]  B. Repp,et al.  Sensorimotor synchronization: A review of recent research (2006–2012) , 2013, Psychonomic Bulletin & Review.

[97]  Rufin VanRullen,et al.  On the cyclic nature of perception in vision versus audition , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[98]  Jeroen van den Brink,et al.  The quantum nature of skyrmions and half-skyrmions in Cu2OSeO3 , 2014, Nature Communications.

[99]  B. Repp,et al.  Synchronization with competing visual and auditory rhythms: bouncing ball meets metronome , 2013, Psychological research.

[100]  S. Kastner,et al.  From Behavior to Neural Dynamics: An Integrated Theory of Attention , 2015, Neuron.

[101]  L. Deouell,et al.  Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment , 2017, PLoS biology.

[102]  Jack J. Lin,et al.  Neural Mechanisms of Sustained Attention Are Rhythmic , 2018, Neuron.

[103]  Kerry Hourigan,et al.  Wake transition of a rolling sphere , 2011, J. Vis..

[104]  Timoteo Carletti,et al.  A minimally invasive neurostimulation method for controlling abnormal synchronisation in the neuronal activity , 2018, PLoS Comput. Biol..

[105]  R. Miall,et al.  Manual tracking of visual targets by trained monkeys , 1986, Behavioural Brain Research.

[106]  J. Devin McAuley,et al.  Attentional entrainment and perceived event duration , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[107]  P. Fries,et al.  Attention Samples Stimuli Rhythmically , 2012, Current Biology.

[108]  C. Schroeder,et al.  The Spectrotemporal Filter Mechanism of Auditory Selective Attention , 2013, Neuron.

[109]  Massimiliano Di Luca,et al.  Temporal Regularity of the Environment Drives Time Perception , 2016, PloS one.

[110]  A. Nobre,et al.  Temporal Expectation Enhances Contrast Sensitivity by Phase Entrainment of Low-Frequency Oscillations in Visual Cortex , 2013, The Journal of Neuroscience.

[111]  Anna C. Nobre,et al.  Anticipated moments: temporal structure in attention , 2017, Nature Reviews Neuroscience.

[112]  Anna C Nobre,et al.  Combining spatial and temporal expectations to improve visual perception. , 2014, Journal of vision.

[113]  Benjamin Morillon,et al.  Organizational principles of multidimensional predictions in human auditory attention , 2018, Scientific Reports.

[114]  Anna Christina Nobre,et al.  Orienting attention to instants in time , 2001, Neuropsychologia.