A dual-pathway neural architecture for specific temporal prediction

Efficient behavior depends in part on the ability to predict the type and the timing of events in the environment. Specific temporal predictions require an internal representation of the temporal structure of events. Here we propose that temporal prediction recruits adaptive and non-adaptive oscillatory mechanisms involved in establishing such an internal representation. Partial structural and functional convergence of the underlying mechanisms allows speculation about an extended subcortico-cortical network. This network develops around a dual-pathway architecture, which establishes the basis for preparing the organism for perceptual integration, for the generation of specific temporal predictions, and for optimizing the brain's allocation of its limited resources. Key to these functions is rapid cerebellar transmission of an adaptively-filtered, event-based representation of temporal structure. Rapid cerebellar transmission engages a pathway comprising connections from early sensory processing stages to the cerebellum and from there to the thalamus, effectively bypassing more central stages of classical sensory pathways.

[1]  James Ashe,et al.  Role of olivocerebellar system in timing without awareness , 2011, Proceedings of the National Academy of Sciences.

[2]  C. Huang,et al.  Organization of the auditory area in the posterior cerebellar vermis of the cat , 2004, Experimental Brain Research.

[3]  Eugenio Rodriguez,et al.  Neural synchrony and the development of cortical networks , 2010, Trends in Cognitive Sciences.

[4]  Fred Cummins,et al.  Oscillators and Syllables: A Cautionary Note , 2012, Front. Psychology.

[5]  Christopher Miall,et al.  The Storage of Time Intervals Using Oscillating Neurons , 1989, Neural Computation.

[6]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. II. Responses to movement triggering vs. nontriggering sensory signals. , 1985, Journal of neurophysiology.

[7]  E. Courchesne,et al.  A new role for the cerebellum in cognitive operations. , 1992, Behavioral neuroscience.

[8]  Karl J. Friston,et al.  Prediction, perception and agency , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  Robert T. Knight,et al.  Making order from chaos: the misguided frontal lobe , 2002, Nature Neuroscience.

[10]  R. Llinás,et al.  Bursting of thalamic neurons and states of vigilance. , 2006, Journal of neurophysiology.

[11]  Masao Ito Control of mental activities by internal models in the cerebellum , 2008, Nature Reviews Neuroscience.

[12]  N. Ramnani The primate cortico-cerebellar system: anatomy and function , 2006, Nature Reviews Neuroscience.

[13]  Erich Schröger,et al.  Temporal aspects of prediction in audition: cortical and subcortical neural mechanisms. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  F. Crick Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Eugene M. Izhikevich,et al.  Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting , 2006 .

[16]  Mitsuo Kawato,et al.  Speech and song: The role of the cerebellum , 2008, The Cerebellum.

[17]  Peter Mariën,et al.  Cerebellar neurocognition: Insights into the bottom of the brain , 2008, Clinical Neurology and Neurosurgery.

[18]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[19]  H. Swadlow,et al.  The impact of 'bursting' thalamic impulses at a neocortical synapse , 2001, Nature Neuroscience.

[20]  S. Sherman The thalamus is more than just a relay , 2007, Current Opinion in Neurobiology.

[21]  Angela R Laird,et al.  Cerebellum and auditory function: An ALE meta‐analysis of functional neuroimaging studies , 2005, Human brain mapping.

[22]  L. Aitkin,et al.  Responses of single units in cerebellar vermis of the cat to monaural and binaural stimuli. , 1975, Journal of neurophysiology.

[23]  J. Freeman Responses of cat cerebellar Purkinje cells to convergent inputs from cerebral cortex and peripheral sensory systems. , 1970, Journal of neurophysiology.

[24]  H. Zelaznik,et al.  Disrupted Timing of Discontinuous But Not Continuous Movements by Cerebellar Lesions , 2003, Science.

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

[26]  Richard S. J. Frackowiak,et al.  Endogenous Cortical Rhythms Determine Cerebral Specialization for Speech Perception and Production , 2007, Neuron.

[27]  Patrícia Maria Sens,et al.  Participation of the cerebellum in auditory processing. , 2007, Brazilian journal of otorhinolaryngology.

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

[29]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[30]  W. Koella,et al.  The cerebellar acoustic response and its interaction with optic responses. , 1961, Electroencephalography and clinical neurophysiology.

[31]  S. Highstein,et al.  Responses of the cerebellar vermis to binaural auditory stimulation. , 1968, Brain research.

[32]  Matthew H. Davis,et al.  Temporal Predictive Codes for Spoken Words in Auditory Cortex , 2012, Current Biology.

[33]  P. Nixon,et al.  The role of the cerebellum in preparing responses to predictable sensory events , 2008, The Cerebellum.

[34]  P. Strick,et al.  Cerebellum and nonmotor function. , 2009, Annual review of neuroscience.

[35]  Edward L. Bartlett,et al.  Neural representations of temporally modulated signals in the auditory thalamus of awake primates. , 2007, Journal of neurophysiology.

[36]  G. Misrahy,et al.  Acoustic cerebellar pathways in cats. , 1961, Journal of neurophysiology.

[37]  P. Strick,et al.  Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output , 2007, The Journal of Neuroscience.

[38]  N. Sawtell,et al.  Cerebellum-like structures and their implications for cerebellar function. , 2008, Annual review of neuroscience.

[39]  John E. Schlerf,et al.  Dedicated and intrinsic models of time perception , 2008, Trends in Cognitive Sciences.

[40]  Ann M Graybiel,et al.  Neural representation of time in cortico-basal ganglia circuits , 2009, Proceedings of the National Academy of Sciences.

[41]  U. Goswami,et al.  Music, rhythm, rise time perception and developmental dyslexia: Perception of musical meter predicts reading and phonology , 2011, Cortex.

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

[43]  R. Snider,et al.  RECEIVING AREAS OF THE TACTILE, AUDITORY, AND VISUAL SYSTEMS IN THE CEREBELLUM , 1944 .

[44]  M. Raichle Two views of brain function , 2010, Trends in Cognitive Sciences.

[45]  L. Trainor Predictive information processing is a fundamental learning mechanism present in early development: evidence from infants. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[46]  X. F. Wang,et al.  The dentate nucleus is a short-latency relay of a primary auditory transmission pathway. , 1991, Neuroreport.

[47]  Sonja A. Kotz,et al.  Functional dissociation of pre-SMA and SMA-proper in temporal processing , 2012, NeuroImage.

[48]  Michael D. Hunter,et al.  The Role of the Cerebellum in Sub- and Supraliminal Error Correction during Sensorimotor Synchronization: Evidence from fMRI and TMS , 2011, Journal of Cognitive Neuroscience.

[49]  G. McCarthy,et al.  Perceiving patterns in random series: dynamic processing of sequence in prefrontal cortex , 2002, Nature Neuroscience.

[50]  J. A. Altman,et al.  Electrical responses of the auditory area of the cerebellar cortex to acoustic stimulation , 1976, Experimental Brain Research.

[51]  Nathaniel B Sawtell,et al.  Neural mechanisms for filtering self-generated sensory signals in cerebellum-like circuits , 2011, Current Opinion in Neurobiology.

[52]  Peter E Keller,et al.  Sensorimotor synchronization with adaptively timed sequences. , 2008, Human movement science.

[53]  S. Murray Sherman,et al.  A wake-up call from the thalamus , 2001, Nature Neuroscience.

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

[55]  M Dennis,et al.  Perception and estimation of time in long-term survivors of childhood posterior fossa tumors , 2000, Journal of the International Neuropsychological Society.

[56]  J. Devin McAuley Perception of time as phase: toward an adaptive-oscillator model of rhythmic pattern processing , 1996 .

[57]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[58]  Peter E. Keller,et al.  Adaptation to tempo changes in sensorimotor synchronization: Effects of intention, attention, and awareness , 2004, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[59]  R. Snider,et al.  THE INTERACTION OF VARIOUS IMPULSES IN THE CEREBELLUM. , 1964, Journal of the neurological sciences.

[60]  A. Nobre,et al.  The Cerebellum Predicts the Timing of Perceptual Events , 2008, The Journal of Neuroscience.

[61]  E. Courchesne,et al.  Prediction and preparation, fundamental functions of the cerebellum. , 1997, Learning & memory.

[62]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[63]  Chun-I Yeh,et al.  Dynamic Encoding of Natural Luminance Sequences by LGN Bursts , 2006, PLoS biology.

[64]  S. Grondin,et al.  From physical time to the first and second moments of psychological time. , 2001, Psychological bulletin.

[65]  W. Meck,et al.  Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. , 2004, Brain research. Cognitive brain research.

[66]  Eric D. Young,et al.  What's a cerebellar circuit doing in the auditory system? , 2004, Trends in Neurosciences.

[67]  J. Velluti,et al.  Cerebellar sensory functions: Rat auditory evoked potentials , 1977, Experimental Neurology.

[68]  Ricarda I. Schubotz,et al.  Prediction, Cognition and the Brain , 2009, Front. Hum. Neurosci..

[69]  Christoph Kayser,et al.  Monkey drumming reveals common networks for perceiving vocal and nonvocal communication sounds , 2009, Proceedings of the National Academy of Sciences.

[70]  Michael Kiefte,et al.  Sensitivity to change in perception of speech , 2003, Speech Commun..

[71]  B. Balas,et al.  Personal Familiarity Influences the Processing of Upright and Inverted Faces in Infants , 2009, Front. Hum. Neurosci..

[72]  Henry J. Alitto,et al.  Dynamic properties of thalamic neurons for vision. , 2005, Progress in brain research.

[73]  A. Nobre,et al.  Top-down modulation: bridging selective attention and working memory , 2012, Trends in Cognitive Sciences.

[74]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[75]  R. Shofer,et al.  Firing patterns induced by sound in single units of the cerebellar cortex , 2004, Experimental Brain Research.

[76]  John F. Kolen,et al.  Resonance and the Perception of Musical Meter , 1994, Connect. Sci..

[77]  Steven Greenberg,et al.  On the Possible Role of Brain Rhythms in Speech Perception: Intelligibility of Time-Compressed Speech with Periodic and Aperiodic Insertions of Silence , 2009, Phonetica.

[78]  C. Woody,et al.  Identification of short latency auditory responsive neurons in the cat dentate nucleus. , 1994, Neuroreport.

[79]  Eugene M. Izhikevich,et al.  Which model to use for cortical spiking neurons? , 2004, IEEE Transactions on Neural Networks.

[80]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[81]  S. Kotz,et al.  Temporal regularity effects on pre-attentive and attentive processing of deviance , 2011, Biological Psychology.

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

[83]  Warren H Meck,et al.  Cortico-striatal Representation of Time in Animals and Humans This Review Comes from a Themed Issue on Cognitive Neuroscience Edited Evidence from Patient Populations and Electrical Potentials Neuroimaging Evidence Using Fmri and Pet , 2022 .

[84]  B. Ross,et al.  Internalized Timing of Isochronous Sounds Is Represented in Neuromagnetic Beta Oscillations , 2012, The Journal of Neuroscience.

[85]  L. Deouell,et al.  Direct evidence for differential roles of temporal and frontal components of auditory change detection , 2007, Neuropsychologia.

[86]  R. Ivry,et al.  The neural representation of time , 2004, Current Opinion in Neurobiology.

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

[88]  A. Puce,et al.  Neuronal oscillations and visual amplification of speech , 2008, Trends in Cognitive Sciences.

[89]  Sophie K. Scott,et al.  The point of P-centres , 1998 .

[90]  I. Nelken Predictive information processing in the brain: the neural perspective. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[91]  Patrick D. Roberts,et al.  Design principles of sensory processing in cerebellum-like structures , 2008, Biological Cybernetics.

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

[93]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[94]  A. Tversky,et al.  Variants of uncertainty , 1982, Cognition.

[95]  R. Burkard,et al.  Frequency sensitivities of auditory neurons in the cerebellum of the cat , 1986, Brain Research.

[96]  B. Repp Sensorimotor synchronization: A review of the tapping literature , 2005, Psychonomic bulletin & review.

[97]  S. Kotz,et al.  Cortical speech processing unplugged: a timely subcortico-cortical framework , 2010, Trends in Cognitive Sciences.

[98]  Patrick D. Roberts,et al.  Model of auditory prediction in the dorsal cochlear nucleus via spike-timing dependent plasticity , 2006, Neurocomputing.

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

[100]  R W Guillery,et al.  The role of the thalamus in the flow of information to the cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[101]  Jochen Kaiser,et al.  P3b Reflects Periodicity in Linguistic Sequences , 2012, PloS one.

[102]  Sun Xinde HRP STUDY OF NEURAL PROJECTIONS OF ACOUSTIC SIGNAL TO THE CEREBELLUM OF ECHOLOCATING BATS , 1990 .

[103]  P. Strick,et al.  The cerebellum communicates with the basal ganglia , 2005, Nature Neuroscience.

[104]  J. Devin McAuley,et al.  Modeling effects of rhythmic context on perceived duration: a comparison of interval and entrainment approaches to short-interval timing. , 2003, Journal of experimental psychology. Human perception and performance.

[105]  Karl J. Friston,et al.  Frontiers in Neuroinformatics , 2022 .

[106]  C. Schroeder,et al.  The Gamma Oscillation: Master or Slave? , 2009, Brain Topography.

[107]  E. Young,et al.  Spectral Edge Sensitivity in Neural Circuits of the Dorsal Cochlear Nucleus , 2005, The Journal of Neuroscience.

[108]  M. R. Jones,et al.  Dynamic attending and responses to time. , 1989, Psychological review.

[109]  D. Poeppel,et al.  Auditory Cortex Tracks Both Auditory and Visual Stimulus Dynamics Using Low-Frequency Neuronal Phase Modulation , 2010, PLoS biology.

[110]  Charles C Lee,et al.  The distributed auditory cortex , 2007, Hearing Research.

[111]  F. Perrin,et al.  Dissociation of temporal and frontal components in the human auditory N1 wave: a scalp current density and dipole model analysis. , 1994, Electroencephalography and clinical neurophysiology.

[112]  Warren H. Meck,et al.  Modality differences in timing and temporal memory throughout the lifespan , 2011, Brain and Cognition.

[113]  Matthew H. Davis,et al.  Neural Oscillations Carry Speech Rhythm through to Comprehension , 2012, Front. Psychology.

[114]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[115]  Iain D. Gilchrist,et al.  Testing a Simplified Method for Measuring Velocity Integration in Saccades Using a Manipulation of Target Contrast , 2011, Front. Psychology.

[116]  E D Young,et al.  WHY DO CATS NEED A DORSAL COCHLEAR NUCLEUS? , 1996, Journal of basic and clinical physiology and pharmacology.

[117]  Rosa H. Huang,et al.  Projections from the cochlear nucleus to the cerebellum , 1982, Brain Research.

[118]  J. Morton,et al.  Perceptual centers (P-centers). , 1976 .

[119]  L. Aitkin The Auditory Midbrain: Structure and Function in the Central Auditory Pathway , 1986 .

[120]  Peter L. Strick,et al.  The Cerebellum and Basal Ganglia are Interconnected , 2010, Neuropsychology Review.

[121]  Tanaka The role of , 2000, Journal of insect physiology.

[122]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[123]  Patrícia Maria Sens,et al.  Participação do cerebelo no processamento auditivo , 2007 .

[124]  Aniruddh D. Patel,et al.  The impact of basal ganglia lesions on sensorimotor synchronization, spontaneous motor tempo, and the detection of tempo changes , 2011, Behavioural Brain Research.

[125]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[126]  S. Sherman,et al.  On the classification of pathways in the auditory midbrain, thalamus, and cortex , 2011, Hearing Research.

[127]  Irene Daum,et al.  Cerebellar contributions to cognitive functions: A progress report after two decades of research , 2008, The Cerebellum.

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

[129]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[130]  E. Vogel,et al.  Interactions between attention and working memory , 2006, Neuroscience.

[131]  Oded Ghitza,et al.  Linking Speech Perception and Neurophysiology: Speech Decoding Guided by Cascaded Oscillators Locked to the Input Rhythm , 2011, Front. Psychology.