Temporal filtering by prefrontal neurons in duration discrimination

Neural imaging studies have revealed that the prefrontal cortex (PFC) participates in time perception. However, actual functional roles remain unclear. We trained two monkeys to perform a duration‐discrimination task, in which two visual cues were presented consecutively for different durations ranging from 0.2 to 2.0 s. The subjects were required to choose the longer cue. We recorded single‐neuron activity from the PFC while the subjects were performing the task. Responsive neurons for the first cue period were extracted and classified through a cluster analysis of firing rate curves. The neuronal activity was categorized as phasic, ramping and sustained patterns. Among them, the phasic activity was the most prevailing. Peak time of the phasic activity was broadly distributed about 0.8 s after cue onset, leading to a natural assumption that the phasic activity was related to cognitive processes. The phasic activity with constant delay after cue onset might function to filter current cue duration with the peak time. The broad distribution of the peak time would indicate that various filtering durations had been prepared for estimating C1 duration. The most frequent peak time was close to the time separating cue durations into long and short. The activity with this peak time might have had a role of filtering in attempted duration discrimination. Our results suggest that the PFC contributes to duration discrimination with temporal filtering in the cue period.

[1]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[2]  J. Staddon.  Interval timing: memory, not a clock , 2005, Trends in Cognitive Sciences.

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

[4]  Mingxiong Huang,et al.  Neural representation of interval encoding and decision making. , 2004, Brain research. Cognitive brain research.

[5]  J. H. Ward.  Hierarchical Grouping to Optimize an Objective Function , 1963 .

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

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

[8]  N. Suga,et al.  Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Tanji,et al.  Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. I. Responses to instructions determining motor responses to forthcoming signals of different modalities. , 1985, Journal of neurophysiology.

[10]  Å. Hellström.  Comparison is not just subtraction: Effects of time- and space-order on subjective stimulus difference , 2003, Perception & psychophysics.

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

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

[13]  S. Wise,et al.  Neuronal activity related to elapsed time in prefrontal cortex. , 2006, Journal of neurophysiology.

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

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

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

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

[18]  T. Hashikawa,et al.  Temporal Integration and Duration Tuning in the Dorsal Zone of Cat Auditory Cortex , 1997, The Journal of Neuroscience.

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

[20]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[21]  H. D. Potter,et al.  Patterns of acoustically evoked discharges of neurons in the mesencephalon of the bullfrog. , 1965, Journal of neurophysiology.

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

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

[24]  P. M. Hartigan,et al.  Computation of the Dip Statistic to Test for Unimodality , 1985 .

[25]  F. Vidal,et al.  Activation of the supplementary motor area and of attentional networks during temporal processing , 2002, Experimental Brain Research.

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

[27]  B. Grothe,et al.  Duration tuning in the mouse auditory midbrain. , 2000, Journal of neurophysiology.

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

[29]  Jordan Grafman,et al.  Distributed neural systems for temporal production: A functional MRI study , 2003, Brain Research Bulletin.

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

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

[32]  Louis Renoult,et al.  Time is a rubberband: neuronal activity in monkey motor cortex in relation to time estimation , 2006, The European journal of neuroscience.

[33]  L. Rüschendorf,et al.  On the Perception of Time , 2009, Gerontology.

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

[35]  Masahiko Inase,et al.  Delay period activity of monkey prefrontal neurones during duration‐discrimination task , 2006, The European journal of neuroscience.

[36]  J. Coull.  fMRI studies of temporal attention: allocating attention within, or towards, time. , 2004, Brain research. Cognitive brain research.

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

[38]  J. Hartigan,et al.  The Dip Test of Unimodality , 1985 .

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

[40]  Daniel Durstewitz,et al.  Self-Organizing Neural Integrator Predicts Interval Times through Climbing Activity , 2003, The Journal of Neuroscience.

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

[42]  Katya Rubia,et al.  A right hemispheric frontocerebellar network for time discrimination of several hundreds of milliseconds , 2003, NeuroImage.

[43]  Ellen Covey,et al.  Duration selectivity of neurons in the inferior colliculus of the big brown bat: tolerance to changes in sound level. , 2005, Journal of neurophysiology.

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

[45]  Y. Sakurai,et al.  Stimulus duration in working memory is represented by neuronal activity in the monkey prefrontal cortex , 2004, The European journal of neuroscience.

[46]  H. Spinnler.  The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

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

[48]  Matthew B. Wall,et al.  Time perception: Manipulation of task difficulty dissociates clock functions from other cognitive demands , 2007, Neuropsychologia.

[49]  M S Malmierca,et al.  Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties. , 2006, Journal of neurophysiology.