Keeping time: Effects of focal frontal lesions

This study examined the performance of 32 normal subjects and 39 patients with focal lesions of the frontal lobes on two simple timing tasks-responding in time with a tone that regularly repeated at a rate of once every 1.5s, and then maintaining the same regular response rhythm without any external stimulus. The hypothesis was that lesions to the right prefrontal cortex would disrupt timing performance. The two main findings were (1) an abnormally high variability in the timing performance (both self-timed and tone-timed) of patients with lesions to the right lateral frontal lobe, particularly involving Brodmann area 45 and subjacent regions of the basal ganglia; (2) an increase in the variability of timing performance as the task continued in patients with lesions to the superior medial regions of the frontal lobe. These findings indicate that the right lateral frontal lobe is crucially involved in the ongoing control of timed behavior, either because of its role in generating time intervals or in monitoring the passage of these intervals. In contrast, the superior medial regions of the frontal lobe are necessary to maintain consistent timing performance over prolonged periods of time.

[1]  S. Keele,et al.  Does the Cerebellum Provide a Common Computation for Diverse Tasks? A Timing Hypothesis a , 1990, Annals of the New York Academy of Sciences.

[2]  Richard B. Ivry,et al.  Effects of focal basal ganglia lesions on timing and force control , 2005, Brain and Cognition.

[3]  Donald T. Stuss,et al.  Aging and Variability in Performance , 1998 .

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

[5]  E. Pöppel,et al.  A hierarchical model of temporal perception , 1997, Trends in Cognitive Sciences.

[6]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

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

[8]  R. Knight,et al.  Cortical Networks Underlying Mechanisms of Time Perception , 1998, The Journal of Neuroscience.

[9]  A. Kristofferson,et al.  The timing of interresponse intervals , 1973 .

[10]  John J. Foxe,et al.  A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. , 2004, Brain research. Cognitive brain research.

[11]  J H Wearden,et al.  Temporal control of rhythmic performance: a comparison between young and old adults. , 2001, Experimental aging research.

[12]  James B. Rowe,et al.  Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory , 2001, NeuroImage.

[13]  J. Mates,et al.  Temporal Integration in Sensorimotor Synchronization , 1994, Journal of Cognitive Neuroscience.

[14]  C. Brunia,et al.  Distribution of slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. , 1988, Electroencephalography and clinical neurophysiology.

[15]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  Alan C. Evans,et al.  Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction , 1998, Journal of Cognitive Neuroscience.

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

[18]  P. Fraisse 6 – Rhythm and Tempo , 1982 .

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

[20]  D. Pandya,et al.  Association pathways of the prefrontal cortex and functional observations , 2002 .

[21]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

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

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

[24]  P. Goldman-Rakic,et al.  A role for inhibition in shaping the temporal flow of information in prefrontal cortex , 2002, Nature Neuroscience.

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

[26]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[27]  Alan M. Wing,et al.  Modeling variability and dependence in timing , 1996 .

[28]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[29]  P A Hancock,et al.  Human aging and duration judgments: a meta-analytic review. , 1998, Psychology and aging.

[30]  P. A. Lewis,et al.  Brain activity correlates differentially with increasing temporal complexity of rhythms during initialisation, synchronisation, and continuation phases of paced finger tapping , 2004, Neuropsychologia.

[31]  John C. Rothwell,et al.  The right dorsolateral prefrontal cortex is essential in time reproduction: an investigation with repetitive transcranial magnetic stimulation , 2004, Experimental Brain Research.

[32]  J. Requin Attention and Performance VII , 1980 .

[33]  W. Meck,et al.  Dissecting the Brain's Internal Clock: How Frontal–Striatal Circuitry Keeps Time and Shifts Attention , 2002, Brain and Cognition.

[34]  Alan C. Evans,et al.  Hearing in the Mind's Ear: A PET Investigation of Musical Imagery and Perception , 1996, Journal of Cognitive Neuroscience.

[35]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[36]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[37]  JORDAN GRAFMAN,et al.  Duration Processing after Frontal Lobe Lesions a , 1995, Annals of the New York Academy of Sciences.

[38]  M. Petrides The role of the mid-dorsolateral prefrontal cortex in working memory , 2000, Experimental Brain Research.

[39]  A. Ferrandez,et al.  ERPs and PET analysis of time perception: Spatial and temporal brain mapping during visual discrimination tasks , 2000, Human brain mapping.

[40]  R. Passingham The frontal lobes and voluntary action , 1993 .

[41]  Richard Ragot,et al.  What is common to brain activity evoked by the perception of visual and auditory filled durations? A study with MEG and EEG co-recordings. , 2004, Brain research. Cognitive brain research.

[42]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Katsunori Kitano,et al.  Time representing cortical activities: two models inspired by prefrontal persistent activity , 2003, Biological Cybernetics.

[44]  Laurent Hugueville,et al.  Neural network involved in time perception: An fMRI study comparing long and short interval estimation , 2005, Human brain mapping.

[45]  M. Bangert,et al.  Brain Processing of Meter and Rhythm in Music , 2003, Annals of the New York Academy of Sciences.

[46]  Richard B. Ivry,et al.  Comparison of patients with Parkinson’s disease or cerebellar lesions in the production of periodic movements involving event-based or emergent timing , 2005, Brain and Cognition.

[47]  Michael Petrides,et al.  The Mid-ventrolateral Prefrontal Cortex and Active Mnemonic Retrieval , 2002, Neurobiology of Learning and Memory.

[48]  Curt Sachs Rhythm and tempo , 1953 .

[49]  R Todd Ogden,et al.  Adding drift to the decomposition of simple isochronous tapping: an extension of the Wing-Kristofferson model. , 2004, Journal of experimental psychology. Human perception and performance.

[50]  D. Cramon,et al.  Time estimation as a neuronal network property: a lesion study , 1997, Neuroreport.

[51]  J. Binder,et al.  Distributed Neural Systems Underlying the Timing of Movements , 1997, The Journal of Neuroscience.

[52]  P. Lewis,et al.  Finding the timer , 2002, Trends in Cognitive Sciences.

[53]  T. Robbins,et al.  A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. , 2004, Brain : a journal of neurology.

[54]  J A Obeso,et al.  Performance of repetitive wrist movements in Parkinson's disease. , 1992, Brain : a journal of neurology.

[55]  M. D’Esposito,et al.  The Influence of Working-Memory Demand and Subject Performance on Prefrontal Cortical Activity , 2002, Journal of Cognitive Neuroscience.

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

[57]  R. Miall,et al.  Brain activation patterns during measurement of sub- and supra-second intervals , 2003, Neuropsychologia.

[58]  Andrew Simmons,et al.  Prefrontal involvement in temporal bridging and timing movement , 1998, Neuropsychologia.

[59]  D. Stuss,et al.  Staying on the job: the frontal lobes control individual performance variability. , 2003, Brain : a journal of neurology.

[60]  A. Halpern,et al.  Cerebral Substrates of Musical Imagery , 2001, Annals of the New York Academy of Sciences.

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

[62]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[63]  Brian Levine,et al.  Fractionalization and localization of distinct frontal lobe processes: Evidence from focal lesions in humans , 2002 .

[64]  A. Kristofferson,et al.  Response delays and the timing of discrete motor responses , 1973 .

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

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

[67]  T. Shallice,et al.  The multiple dimensions of sustained attention , 2008, Cortex.

[68]  Roland R. Lee,et al.  Does the representation of time depend on the cerebellum? Effect of cerebellar stroke. , 2003, Brain : a journal of neurology.

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

[70]  D. Deutsch,et al.  The Psychology of Music , 1983 .

[71]  A. Wing Voluntary Timing and Brain Function: An Information Processing Approach , 2002, Brain and Cognition.

[72]  T. Shallice,et al.  A Multidisciplinary Approach to Anterior Attentional Functions a , 1995, Annals of the New York Academy of Sciences.

[73]  M. Jahanshahi,et al.  Time estimation and reproduction is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

[74]  S. Petersen,et al.  Direct Comparison of Prefrontal Cortex Regions Engaged by Working and Long-Term Memory Tasks , 2001, NeuroImage.

[75]  Sara Torriero,et al.  Underestimation of time perception after repetitive transcranial magnetic stimulation , 2003, Neurology.

[76]  B. Milner,et al.  Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man , 1982, Neuropsychologia.

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

[78]  Richard B. Ivry,et al.  Neural mechanisms of timing , 1997, Trends in Cognitive Sciences.

[79]  G. Madison,et al.  Variability in isochronous tapping: higher order dependencies as a function of intertap interval. , 2001, Journal of experimental psychology. Human perception and performance.

[80]  Tim Shallice,et al.  Fractionation of the supervisory system. , 2002 .

[81]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[82]  P. Goldman-Rakic,et al.  Human Brain Mapping 6:14–32(1998) � Dissociation of Mnemonic and Perceptual Processes During Spatial and Nonspatial Working Memory Using fMRI , 2022 .

[83]  P. Maquet,et al.  The basic pattern of activation in motor and sensory temporal tasks: positron emission tomography data , 1997, Neuroscience Letters.

[84]  E T Rolls,et al.  Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. , 2004, Brain : a journal of neurology.

[85]  D. Stuss,et al.  Stroop performance in focal lesion patients: dissociation of processes and frontal lobe lesion location , 2001, Neuropsychologia.

[86]  Ewald Moser,et al.  The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response , 2003, NeuroImage.

[87]  T Shallice,et al.  Impaired concentration due to frontal lobe damage from two distinct lesion sites , 2005, Neurology.

[88]  L. A. Jeffress,et al.  Cerebral Mechanisms in Behavior , 1953 .

[89]  F. W. Cody,et al.  The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson's disease. , 1996, Brain : a journal of neurology.

[90]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[91]  Robert T. Knight,et al.  Contributions of Subregions of the Prefrontal Cortex to Working Memory: Evidence from Brain Lesions in Humans , 2002, Journal of Cognitive Neuroscience.

[92]  T. Shallice,et al.  Multiple frontal systems controlling response speed , 2005, Neuropsychologia.