Time is a rubberband: neuronal activity in monkey motor cortex in relation to time estimation

Anticipation of predictable events is crucial for organizing motor performance. Using instructed delay tasks, it has been shown that even when delay duration is kept constant, reaction time fluctuates from trial to trial. As time estimation is at the core of anticipatory behavior, it is reasonable to speculate whether neuronal delay activity correlates with the subjective estimate of time. As a consequence of the scalar property of time estimation processes, the variability in time estimation increases continuously as time passes during the delay. This scalar property may then be reflected in the increasing variability in neuronal delay activity. We thus studied the influence of temporal prior information on neuronal delay activity in monkey motor cortex in two conceptually different tasks in which two equally probable delay durations were randomly presented. We hypothesized that if one considers the animal's subjective time as the time which elapses between the first (instruction) signal and movement onset, then, by suppressing this temporal variability, across‐trial variability in neuronal discharge should decrease. We thus defined a new time scale in each trial such that, after rescaling, the time between the instruction signal and movement onset was identical in all trials. Each spike was then displaced in time accordingly. As expected, the variability in the timing of neuronal peak discharges no longer increased during the trial. This suggests a direct link between the temporal profile of spiking activity and time estimation. The timing of motor cortical activity reflected the ‘elasticity’ of the animal's subjective time.

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

[2]  A. Riehle,et al.  The predictive value for performance speed of preparatory changes in neuronal activity of the monkey motor and premotor cortex , 1993, Behavioural Brain Research.

[3]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[4]  Nicolas Brunel,et al.  Dynamics and plasticity of stimulus-selective persistent activity in cortical network models. , 2003, Cerebral cortex.

[5]  M. Shadlen,et al.  A representation of the hazard rate of elapsed time in macaque area LIP , 2005, Nature Neuroscience.

[6]  R. Romo,et al.  Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. , 2003, Cerebral cortex.

[7]  W. T. Thach Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. , 1978, Journal of neurophysiology.

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

[9]  M. Coles,et al.  Handbook of cognitive psychophysiology : central and autonomic nervous system approaches , 1991 .

[10]  Alexa Riehle,et al.  Preparation for Action: one of the Key Functions of Motor Cortex , 2004 .

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

[12]  Eilon Vaadia,et al.  Motor Cortex in Voluntary Movements: A Distributed System for Distributed Functions , 2007 .

[13]  E V Evarts,et al.  Precentral and postcentral cortical activity in association with visually triggered movement. , 1974, Journal of neurophysiology.

[14]  Kisou Kubota,et al.  Preparatory activity of monkey pyramidal tract neurons related to quick movement onset during visual tracking performance , 1979, Brain Research.

[15]  P. Goldman-Rakic Regional and cellular fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[16]  D. Boussaoud,et al.  Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. , 2002, Journal of neurophysiology.

[17]  M. Shadlen,et al.  Microstimulation of visual cortex affects the speed of perceptual decisions , 2003, Nature Neuroscience.

[18]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[19]  Stefan Rotter,et al.  Single-trial estimation of neuronal firing rates: From single-neuron spike trains to population activity , 1999, Journal of Neuroscience Methods.

[20]  S. Wise,et al.  Premotor cortex of the rhesus monkey: neuronal activity in anticipation of predictable environmental events , 2004, Experimental Brain Research.

[21]  Sonja Grün,et al.  Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation , 2000, Journal of Physiology-Paris.

[22]  E. Schmidt,et al.  Cortical cell discharge patterns in anticipation of a trained movement. , 1974, Brain research.

[23]  Masataka Watanabe,et al.  Prefrontal and cingulate unit activity during timing behavior in the monkey , 1979, Brain Research.

[24]  P. Matthews,et al.  Neurophysiological approaches to higher brain functions E. V. Evarts, Y. Shinoda and S. P. Wise. Wiley and Sons, New York (1984). 198 pp., cloth £40.90 , 1986, Neuroscience.

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

[26]  D P Munoz,et al.  Neuronal Correlates for Preparatory Set Associated with Pro-Saccades and Anti-Saccades in the Primate Frontal Eye Field , 2000, The Journal of Neuroscience.

[27]  A. Georgopoulos Higher order motor control. , 1991, Annual review of neuroscience.

[28]  Alexa Riehle,et al.  Spike synchronization and firing rate in a population of motor cortical neurons in relation to movement direction and reaction time , 2003, Biological Cybernetics.

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

[30]  Alexa Riehle,et al.  Preparation for Action : one of the Key Functions of Motor Cortex , 2004 .

[31]  G. Schöner,et al.  Preshaping and continuous evolution of motor cortical representations during movement preparation , 2003, The European journal of neuroscience.

[32]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

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

[34]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

[35]  J. Tanji,et al.  Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. , 1976, Journal of neurophysiology.

[36]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[37]  Cristina Lucchetti,et al.  Time-modulated neuronal activity in the premotor cortex of macaque monkeys , 2001, Experimental Brain Research.

[38]  D. Munoz,et al.  Saccadic Probability Influences Motor Preparation Signals and Time to Saccadic Initiation , 1998, The Journal of Neuroscience.

[39]  S. Wise,et al.  Neuronal activity preceding directional and nondirectional cues in the premotor cortex of rhesus monkeys. , 1988, Somatosensory & motor research.

[40]  Alexa Riehle,et al.  Context‐related representation of timing processes in monkey motor cortex , 2003, The European journal of neuroscience.

[41]  R B Ivry,et al.  Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. , 1998, Brain research. Cognitive brain research.

[42]  J. Requin,et al.  Changes in neuronal activity of the monkey precentral cortex during preparation for movement. , 1986, Journal of neurophysiology.

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

[44]  M. Shadlen,et al.  A role for neural integrators in perceptual decision making. , 2003, Cerebral cortex.