How noise contributes to time-scale invariance of interval timing.

Time perception in the suprasecond range is crucial for fundamental cognitive processes such as decision making, rate calculation, and planning. In the vast majority of species, behavioral manipulations, and neurophysiological manipulations, interval timing is scale invariant: the time-estimation errors are proportional to the estimated duration. The origin and mechanisms of this fundamental property are unknown. We discuss the computational properties of a circuit consisting of a large number of (input) neural oscillators projecting on a small number of (output) coincidence detector neurons, which allows time to be coded by the pattern of coincidental activation of its inputs. We show that time-scale invariance emerges from the neural noise, such as small fluctuations in the firing patterns of its input neurons and in the errors with which information is encoded and retrieved by its output neurons. In this architecture, time-scale invariance is resistant to manipulations as it depends neither on the details of the input population nor on the distribution probability of noise.

[1]  Claudette Fortin,et al.  Short-term memory and time estimation: beyond the 2-second "critical" value. , 2002, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[2]  C. Stevens,et al.  Synaptic noise and other sources of randomness in motoneuron interspike intervals. , 1968, Journal of neurophysiology.

[3]  William L. Ditto,et al.  Temporal spike pattern learning. , 2008 .

[4]  J. Gibbon,et al.  Scalar expectancy theory and peak-interval timing in humans. , 1998, Journal of experimental psychology. Animal behavior processes.

[5]  F. Vidal,et al.  Functional Anatomy of the Attentional Modulation of Time Estimation , 2004, Science.

[6]  J. Xu,et al.  Global dynamics and stochastic resonance of the forced FitzHugh-Nagumo neuron model. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[7]  D. Durstewitz,et al.  The ability of the mesocortical dopamine system to operate in distinct temporal modes , 2007, Psychopharmacology.

[8]  Rickey E Carter,et al.  Interval timing accuracy and scalar timing in C57BL/6 mice. , 2009, Behavioral neuroscience.

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

[10]  C. Buhusi,et al.  Differential effects of methamphetamine and haloperidol on the control of an internal clock. , 2002, Behavioral neuroscience.

[11]  D. Buonomano,et al.  The neural basis of temporal processing. , 2004, Annual review of neuroscience.

[12]  James G. Herndon,et al.  Anatomical specificity within rat striatum for the dopaminergic modulation of DRL responding and activity , 1978, Brain Research.

[13]  J Staddon,et al.  Time, trace, memory. , 1999, Journal of the experimental analysis of behavior.

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

[15]  W. Meck,et al.  Peak-interval timing in humans activates frontal-striatal loops , 1996, NeuroImage.

[16]  J. Wearden,et al.  More is not necessarily better: Examining the nature of the temporal reference memory component in timing , 2003, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[17]  Marc Benayoun,et al.  Avalanches in a Stochastic Model of Spiking Neurons , 2010, PLoS Comput. Biol..

[18]  P. Killeen,et al.  A behavioral theory of timing , 1988 .

[19]  S. Grossberg,et al.  A neural network model of adaptively timed reinforcement learning and hippocampal dynamics. , 1992, Brain research. Cognitive brain research.

[20]  C. Morris,et al.  Voltage oscillations in the barnacle giant muscle fiber. , 1981, Biophysical journal.

[21]  J. Gibbon Scalar expectancy theory and Weber's law in animal timing. , 1977 .

[22]  W. Meck,et al.  Neuroimaging of interval timing. , 2004, Brain research. Cognitive brain research.

[23]  J. Paul Bolam,et al.  Cortical and Thalamic Innervation of Direct and Indirect Pathway Medium-Sized Spiny Neurons in Mouse Striatum , 2010, The Journal of Neuroscience.

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

[25]  S. Roberts,et al.  Isolation of an internal clock. , 1981, Journal of experimental psychology. Animal behavior processes.

[26]  M. Nicolelis,et al.  Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. , 2003, Behavioral neuroscience.

[27]  J ANLIKER Variations in Alpha Voltage of the Electroencephalogram and Time Perception , 1963, Science.

[28]  R. Church,et al.  Application of scalar timing theory to individual trials. , 1994 .

[29]  R M Church,et al.  Scalar Timing in Memory , 1984, Annals of the New York Academy of Sciences.

[30]  W. Meck Selective adjustment of the speed of internal clock and memory processes. , 1983, Journal of experimental psychology. Animal behavior processes.

[31]  Arif Babul,et al.  Neuron dynamics in the presence of 1/f noise. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[32]  Charles J. Wilson,et al.  Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo , 1998, Nature.

[33]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[34]  Leslie M Kay,et al.  How global are olfactory bulb oscillations? , 2010, Journal of neurophysiology.

[35]  W. Senn,et al.  Climbing Neuronal Activity as an Event-Based Cortical Representation of Time , 2004, The Journal of Neuroscience.

[36]  A. Hodgkin The local electric changes associated with repetitive action in a non‐medullated axon , 1948, The Journal of physiology.

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

[38]  B. Litt,et al.  High-frequency oscillations and seizure generation in neocortical epilepsy. , 2004, Brain : a journal of neurology.

[39]  C. Buhusi,et al.  Modeling Pharmacological Clock and Memory Patterns of Interval Timing in a Striatal Beat-Frequency Model with Realistic, Noisy Neurons , 2011, Front. Integr. Neurosci..

[40]  K. Schäfer,et al.  Oscillation and noise determine signal transduction in shark multimodal sensory cells , 1994, Nature.

[41]  X. Leinekugel,et al.  Neural circuits underlying the generation of theta oscillations , 2012, Journal of Physiology-Paris.

[42]  Jonathan D. Cohen,et al.  A Model of Interval Timing by Neural Integration , 2011, The Journal of Neuroscience.

[43]  D. Contreras,et al.  Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex , 2005, Nature Neuroscience.

[44]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

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

[46]  D. Harrington,et al.  Neural Underpinnings of Temporal Processing: Α Review of Focal Lesion, Pharmacological, and Functional Imaging Research , 1999, Reviews in the neurosciences.

[47]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[48]  Charles J. Wilson,et al.  Dynamic Spike Threshold and Zero Membrane Slope Conductance Shape the Response of Subthalamic Neurons to Cortical Input , 2010, The Journal of Neuroscience.

[49]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[50]  Henry D I Abarbanel,et al.  Neural circuitry for recognizing interspike interval sequences. , 2006, Physical review letters.

[51]  J. Staddon,et al.  Time and memory: towards a pacemaker-free theory of interval timing. , 1999, Journal of the experimental analysis of behavior.

[52]  W. Meck,et al.  Differential modulation of clock speed by the administration of intermittent versus continuous cocaine. , 2004, Behavioral neuroscience.

[53]  Alex Kacelnik,et al.  Optimal foraging and timing processes in the starling, Sturnus vulgaris: effect of inter-capture interval , 1992, Animal Behaviour.

[54]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[55]  Entraining the topology and the dynamics of a network of phase oscillators. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[56]  C. Buhusi,et al.  Timing in simple conditioning and occasion setting: a neural network approach , 1999, Behavioural Processes.

[57]  J. Gibbon,et al.  Coupled Temporal Memories in Parkinson's Disease: A Dopamine-Related Dysfunction , 1998, Journal of Cognitive Neuroscience.

[58]  P R Killeen,et al.  How the propagation of error through stochastic counters affects time discrimination and other psychophysical judgments. , 2000, Psychological review.

[59]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

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

[61]  E. E. Fetz,et al.  Sustained excitatory synaptic input to motor cortex neurons in awake animals revealed by intracellular recording of membrane potentials , 2004, Experimental Brain Research.

[62]  A. Grinvald,et al.  Spontaneously emerging cortical representations of visual attributes , 2003, Nature.

[63]  R. Church,et al.  Alternative representations of time, number, and rate , 1990, Cognition.

[64]  T. Sejnowski,et al.  Discovering Spike Patterns in Neuronal Responses , 2004, The Journal of Neuroscience.

[65]  J. White,et al.  Channel noise in neurons , 2000, Trends in Neurosciences.

[66]  Xin Jin,et al.  Start/stop signals emerge in nigrostriatal circuits during sequence learning , 2010, Nature.

[67]  N. Kopell,et al.  Olfactory Bulb Gamma Oscillations Are Enhanced with Task Demands , 2007, The Journal of Neuroscience.

[68]  C. Stevens,et al.  Input synchrony and the irregular firing of cortical neurons , 1998, Nature Neuroscience.

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

[70]  J. Wearden,et al.  Double standards: Memory loading in temporal reference memory , 2004, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[71]  M. Kahana,et al.  Reset of human neocortical oscillations during a working memory task , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[72]  R. Church,et al.  Nucleus basalis magnocellularis and medial septal area lesions differentially impair temporal memory , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  V. Calhoun,et al.  Functional neural circuits for mental timekeeping , 2007, Human brain mapping.

[74]  A. Faisal,et al.  Noise in the nervous system , 2008, Nature Reviews Neuroscience.

[75]  Vincenzo Crunelli,et al.  Infraslow (<0.1 Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. , 2011, Progress in brain research.

[76]  A. Machado Learning the temporal dynamics of behavior. , 1997, Psychological review.

[77]  H. Gurden,et al.  Alteration of sensory-evoked metabolic and oscillatory activities in the olfactory bulb of GLAST-deficient mice , 2012, Front. Neural Circuits.

[78]  Bard Ermentrout,et al.  Type I Membranes, Phase Resetting Curves, and Synchrony , 1996, Neural Computation.

[79]  J. Wearden,et al.  Short-term memory for time in children and adults: A behavioral study and a model. , 2007, Journal of experimental child psychology.

[80]  G. Buzsáki Theta Oscillations in the Hippocampus , 2002, Neuron.

[81]  Terrence J. Sejnowski,et al.  Irregular Firing of Isolated Cortical Interneurons in Vitro Driven by Intrinsic Stochastic Mechanisms , 2008, Neural Computation.

[82]  C. Gallistel,et al.  Time, rate, and conditioning. , 2000, Psychological review.

[83]  Hildegard Meyer-Ortmanns,et al.  Noise as control parameter in networks of excitable media: Role of the network topology. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[84]  U. Karmarkar,et al.  Timing in the Absence of Clocks: Encoding Time in Neural Network States , 2007, Neuron.