The neural basis of temporal processing.

A complete understanding of sensory and motor processing requires characterization of how the nervous system processes time in the range of tens to hundreds of milliseconds (ms). Temporal processing on this scale is required for simple sensory problems, such as interval, duration, and motion discrimination, as well as complex forms of sensory processing, such as speech recognition. Timing is also required for a wide range of motor tasks from eyelid conditioning to playing the piano. Here we review the behavioral, electrophysiological, and theoretical literature on the neural basis of temporal processing. These data suggest that temporal processing is likely to be distributed among different structures, rather than relying on a centralized timing area, as has been suggested in internal clock models. We also discuss whether temporal processing relies on specialized neural mechanisms, which perform temporal computations independent of spatial ones. We suggest that, given the intricate link between temporal and spatial information in most sensory and motor tasks, timing and spatial processing are intrinsic properties of neural function, and specialized timing mechanisms such as delay lines, oscillators, or a spectrum of different time constants are not required. Rather temporal processing may rely on state-dependent changes in network dynamics.

[1]  G. Holmes THE CEREBELLUM OF MAN , 1939 .

[2]  K. Lashley The problem of serial order in behavior , 1951 .

[3]  A. Liberman,et al.  Tempo of frequency change as a cue for distinguishing classes of speech sounds. , 1956, Journal of experimental psychology.

[4]  R. Dow,et al.  The Physiology and Pathology of the Cerebellum , 1958 .

[5]  C. Douglas Creelman,et al.  Human Discrimination of Auditory Duration , 1962 .

[6]  M. Treisman Temporal discrimination and the indifference interval. Implications for a model of the "internal clock". , 1963, Psychological monographs.

[7]  L. Lisker,et al.  A Cross-Language Study of Voicing in Initial Stops: Acoustical Measurements , 1964 .

[8]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[9]  M Ito,et al.  Neurophysiological aspects of the cerebellar motor control system. , 1970, International journal of neurology.

[10]  I. Lehiste,et al.  Role of duration in disambiguating syntactically ambiguous sentences , 1975 .

[11]  David J. Getty,et al.  Discrimination of short temporal intervals: A comparison of two models , 1975 .

[12]  Pierre L. Divenyi,et al.  Discrimination of time intervals marked by brief acoustic pulses of various intensities and spectra , 1977 .

[13]  J. R. Millenson,et al.  Classical conditioning of the rabbit's nictitating membrane response under fixed and mixed CS-US intervals , 1977 .

[14]  A. Liberman,et al.  Some experiments on the sound of silence in phonetic perception. , 1979, The Journal of the Acoustical Society of America.

[15]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  W. Sullivan,et al.  Possible neural mechanisms of target distance coding in auditory system of the echolocating bat Myotis lucifugus. , 1982, Journal of neurophysiology.

[17]  D. Margoliash Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  Robert Rousseau,et al.  Duration discrimination of empty time intervals marked by intermodal pulses , 1983, Perception & psychophysics.

[19]  M J Bastiani,et al.  Loss of axons in the cat optic nerve following fetal unilateral enucleation: an electron microscopic analysis , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  R. Nicoll,et al.  A bicuculline‐resistant inhibitory post‐synaptic potential in rat hippocampal pyramidal cells in vitro. , 1984, The Journal of physiology.

[21]  G. Klump,et al.  Use of non-arbitrary acoustic criteria in mate choice by female gray tree frogs , 1987, Nature.

[22]  Stephen Grossberg,et al.  Neural dynamics of adaptive timing and temporal discrimination during associative learning , 1989, Neural Networks.

[23]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

[24]  Norman M. Weinberger,et al.  Responses of single auditory cortical neurons to tone sequences , 1989, Brain Research.

[25]  M Dorman,et al.  Consonant recognition as a function of the number of channels of stimulation by patients who use the Symbion cochlear implant. , 1989, Ear and hearing.

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

[27]  G. Lynch,et al.  The neurobiology of learning and memory , 1989, Cognition.

[28]  S. Keele,et al.  Timing Functions of The Cerebellum , 1989, Journal of Cognitive Neuroscience.

[29]  D. Prince,et al.  Frequency‐dependent depression of inhibition in guinea‐pig neocortex in vitro by GABAB receptor feed‐back on GABA release. , 1989, The Journal of physiology.

[30]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex. I. Stimulus-response relations. , 1990, Journal of neurophysiology.

[31]  S. Grondin,et al.  Judging the relative duration of multimodal short empty time intervals , 1991, Perception & psychophysics.

[32]  M. Livingstone,et al.  Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[33]  A. Doupe,et al.  Song-selective auditory circuits in the vocal control system of the zebra finch. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[34]  B J Richmond,et al.  Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. , 1991, Science.

[35]  J. Hore,et al.  Cerebellar dysmetria at the elbow, wrist, and fingers. , 1991, Journal of neurophysiology.

[36]  R. Ivry,et al.  Impaired Velocity Perception in Patients with Lesions of the Cerebellum , 1991, Journal of Cognitive Neuroscience.

[37]  John W. Moore,et al.  A Mechanism for Timing Conditioned Responses , 1992 .

[38]  D. Margoliash,et al.  Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  M. Kawato,et al.  The cerebellum and VOR/OKR learning models , 1992, Trends in Neurosciences.

[40]  T H Rammsayer,et al.  Pharmacologic properties of the internal clock underlying time perception in humans. , 1992, Neuropsychobiology.

[41]  Thomas Rammsayer,et al.  Effects of benzodiazepine‐induced sedation on temporal processing , 1992 .

[42]  J A Obeso,et al.  Temporal discrimination is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

[43]  M. Mauk,et al.  Learning-dependent timing of Pavlovian eyelid responses: differential conditioning using multiple interstimulus intervals. , 1992, Behavioral neuroscience.

[44]  M. Mauk,et al.  Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  C E Carr,et al.  Processing of temporal information in the brain. , 1993, Annual review of neuroscience.

[46]  J. H. Casseday,et al.  Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. , 1994, Science.

[47]  D. M. Green,et al.  A panoramic code for sound location by cortical neurons. , 1994, Science.

[48]  T. Rammsayer,et al.  Effects of practice and signal energy on duration discrimination of brief auditory intervals , 1994, Perception & psychophysics.

[49]  Paula Tallal In the Perception of Speech Time is of the Essence , 1994 .

[50]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[51]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[52]  M. Jüptner,et al.  Localization of a cerebellar timing process using PET , 1995, Neurology.

[53]  M M Merzenich,et al.  Temporal information transformed into a spatial code by a neural network with realistic properties , 1995, Science.

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

[55]  Mark Nawrot,et al.  Motion perception deficits from midline cerebellar lesions in human , 1995, Vision Research.

[56]  R. Klein,et al.  The evidence for a temporal processing deficit linked to dyslexia: A review , 1995, Psychonomic bulletin & review.

[57]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

[58]  R. Ivry The representation of temporal information in perception and motor control , 1996, Current Opinion in Neurobiology.

[59]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[60]  W. Meck Neuropharmacology of timing and time perception. , 1996, Brain research. Cognitive brain research.

[61]  G. Laurent,et al.  Temporal Representations of Odors in an Olfactory Network , 1996, The Journal of Neuroscience.

[62]  S. Lisberger,et al.  The Cerebellum: A Neuronal Learning Machine? , 1996, Science.

[63]  J. Mazziotta,et al.  Brain Activation Induced by Estimation of Duration: A PET Study , 1996, NeuroImage.

[64]  R. Woods,et al.  Abnormal processing of visual motion in dyslexia revealed by functional brain imaging , 1996, Nature.

[65]  S. Grossberg,et al.  Metabotropic Glutamate Receptor Activation in Cerebellar Purkinje Cells as Substrate for Adaptive Timing of the Classically Conditioned Eye-Blink Response , 1996, The Journal of Neuroscience.

[66]  M S Lewicki,et al.  Hierarchical Organization of Auditory Temporal Context Sensitivity , 1996, The Journal of Neuroscience.

[67]  M. Dorman,et al.  Speech intelligibility as a function of the number of channels of stimulation for signal processors using sine-wave and noise-band outputs. , 1997, The Journal of the Acoustical Society of America.

[68]  D. Buonomano,et al.  Learning and Generalization of Auditory Temporal–Interval Discrimination in Humans , 1997, The Journal of Neuroscience.

[69]  N. Donegan,et al.  A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. , 1997, Learning & memory.

[70]  斉藤勲 Long Delay Lines for Ranging Are Created by inhibition in the Inferior Colliculus of the Mustached Bat(ヒゲコウモリが標的との距離測定に必要とする、大脳皮質聴覚野上の遅延線に対する、下丘における抑制性介存神経の関与について) , 1997 .

[71]  JOHN W. Moore,et al.  The TD Model of Classical Conditioning: Response Topography and Brain Implementation , 1997 .

[72]  A. Arnold,et al.  Developmental plasticity in neural circuits for a learned behavior. , 1997, Annual review of neuroscience.

[73]  A. Doupe Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development , 1997, The Journal of Neuroscience.

[74]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[75]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[76]  T. Rammsayer,et al.  Are there dissociable roles of the mesostriatal and mesolimbocortical dopamine systems on temporal information processing in humans? , 1997, Neuropsychobiology.

[77]  C. Gallistel,et al.  Toward a neurobiology of temporal cognition: advances and challenges , 1997, Current Opinion in Neurobiology.

[78]  E Ahissar,et al.  Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Gary J. Rose,et al.  Long-term temporal integration in the anuran auditory system , 1998, Nature Neuroscience.

[80]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.

[81]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[82]  Ehud Ahissar,et al.  Temporal-Code to Rate-Code Conversion by Neuronal Phase-Locked Loops , 1998, Neural Computation.

[83]  S. Hooper Transduction of temporal patterns by single neurons , 1998, Nature Neuroscience.

[84]  D. Harrington,et al.  Temporal processing in the basal ganglia. , 1998, Neuropsychology.

[85]  M. Kilgard,et al.  Plasticity of temporal information processing in the primary auditory cortex , 1998, Nature Neuroscience.

[86]  F Mechler,et al.  Robust Temporal Coding of Contrast by V1 Neurons for Transient But Not for Steady-State Stimuli , 1998, The Journal of Neuroscience.

[87]  Nancy Byl,et al.  Practice-Related Improvements in Somatosensory Interval Discrimination Are Temporally Specific But Generalize across Skin Location, Hemisphere, and Modality , 1998, The Journal of Neuroscience.

[88]  E. Vaadia,et al.  Spatiotemporal structure of cortical activity: properties and behavioral relevance. , 1998, Journal of neurophysiology.

[89]  M. Mauk,et al.  Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses , 1998, Neuropharmacology.

[90]  F. Macar,et al.  Sensory effects on judgments of short time-intervals , 1998, Psychological research.

[91]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[92]  M M Merzenich,et al.  Net interaction between different forms of short-term synaptic plasticity and slow-IPSPs in the hippocampus and auditory cortex. , 1998, Journal of neurophysiology.

[93]  Dean V. Buonomano,et al.  A Neural Network Model of Temporal Code Generation and Position-Invariant Pattern Recognition , 1999, Neural Computation.

[94]  Gerald Westheimer,et al.  Discrimination of short time intervals by the human observer , 1999, Experimental Brain Research.

[95]  J. H. Casseday,et al.  Timing in the auditory system of the bat. , 1999, Annual review of physiology.

[96]  N. Chater The Search for Simplicity: A Fundamental Cognitive Principle? , 1999 .

[97]  T. Rammsayer,et al.  Neuropharmacological Evidence for Different Timing Mechanisms in Humans , 1999, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[98]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[99]  R. Mooney Different Subthreshold Mechanisms Underlie Song Selectivity in Identified HVc Neurons of the Zebra Finch , 2000, The Journal of Neuroscience.

[100]  W. Meck,et al.  Neuropsychological mechanisms of interval timing behavior. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[101]  John M. Beggs,et al.  Prolonged synaptic integration in perirhinal cortical neurons. , 2000, Journal of neurophysiology.

[102]  Javier F. Medina,et al.  Timing Mechanisms in the Cerebellum: Testing Predictions of a Large-Scale Computer Simulation , 2000, The Journal of Neuroscience.

[103]  P. Thier,et al.  Encoding of movement time by populations of cerebellar Purkinje cells , 2000, Nature.

[104]  Robert A. Jacobs,et al.  Motor timing learned without motor training , 2000, Nature Neuroscience.

[105]  Gary J. Rose,et al.  Integration and recovery processes contribute to the temporal selectivity of neurons in the midbrain of the northern leopard frog, Rana pipiens , 2000, Journal of Comparative Physiology A.

[106]  Javier F. Medina,et al.  Computer simulation of cerebellar information processing , 2000, Nature Neuroscience.

[107]  D V Buonomano,et al.  Decoding Temporal Information: A Model Based on Short-Term Synaptic Plasticity , 2000, The Journal of Neuroscience.

[108]  D. P. King,et al.  Molecular genetics of circadian rhythms in mammals. , 2000, Annual review of neuroscience.

[109]  Yasuyoshi Watanabe,et al.  Cortical Networks Recruited for Time Perception: A Monkey Positron Emission Tomography (PET) Study , 2001, NeuroImage.

[110]  E. D’Angelo,et al.  Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum , 2001, Nature Neuroscience.

[111]  Armin Schnider,et al.  Time estimation in Parkinson's disease: normal long duration estimation despite impaired short duration discrimination , 2001, Journal of Neurology.

[112]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[113]  Dean V Buonomano,et al.  Book Review: How Do We Tell Time? , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[114]  S. Hooper,et al.  A computational role for slow conductances: single-neuron models that measure duration , 2002, Nature Neuroscience.

[115]  Eliot A. Brenowitz,et al.  Pacific treefrogs use temporal integration to differentiate advertisement from encounter calls , 2002, Animal Behaviour.

[116]  Michael P. Kilgard,et al.  Order-sensitive plasticity in adult primary auditory cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[117]  Stephen McAdams,et al.  The neuroanatomical substrate of sound duration discrimination , 2002, Neuropsychologia.

[118]  Christian Gaser,et al.  Processing of temporal information and the basal ganglia: new evidence from fMRI , 2003, Experimental Brain Research.

[119]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[120]  Peter König,et al.  Invariant representations of visual patterns in a temporal population code , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[121]  Richard Hans Robert Hahnloser,et al.  An ultra-sparse code underliesthe generation of neural sequences in a songbird , 2002, Nature.

[122]  Henry Markram,et al.  Real-Time Computing Without Stable States: A New Framework for Neural Computation Based on Perturbations , 2002, Neural Computation.

[123]  M. Mauk,et al.  What the cerebellum computes , 2003, Trends in Neurosciences.

[124]  D. Margoliash,et al.  Neuronal populations and single cells representing learned auditory objects , 2003, Nature.

[125]  Dean V Buonomano,et al.  Timing of neural responses in cortical organotypic slices , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[127]  M. Shadlen,et al.  Representation of Time by Neurons in the Posterior Parietal Cortex of the Macaque , 2003, Neuron.

[128]  U. Karmarkar,et al.  Temporal specificity of perceptual learning in an auditory discrimination task. , 2003, Learning & memory.

[129]  O. Creutzfeldt,et al.  Neuronal activity in the human lateral temporal lobe , 1989, Experimental Brain Research.

[130]  J. W. Moore,et al.  Adaptive timing in neural networks: The conditioned response , 1988, Biological Cybernetics.

[131]  O. Creutzfeldt,et al.  Neuronal activity in the human lateral temporal lobe , 2004, Experimental Brain Research.

[132]  Richard Granger,et al.  Computation of frequency-to-spatial transform by olfactory bulb glomeruli , 2004, Biological Cybernetics.

[133]  E. Boyden,et al.  Cerebellum-dependent learning: the role of multiple plasticity mechanisms. , 2004, Annual review of neuroscience.

[134]  S. Keele,et al.  Dissociation of the lateral and medial cerebellum in movement timing and movement execution , 2004, Experimental Brain Research.

[135]  C. Malsburg Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.