Functional Development of Fronto-Striato-Parietal Networks Associated with Time Perception

Compared to our understanding of the functional maturation of executive functions, little is known about the neurofunctional development of perceptive functions. Time perception develops during late adolescence, underpinning many functions including motor and verbal processing, as well as late maturing higher order cognitive skills such as forward planning and future-related decision making. Nothing, however, is known about the neurofunctional changes associated with time perception from childhood to adulthood. Using functional magnetic resonance imaging we explored the effects of age on the brain activation and functional connectivity of 32 male participants from 10 to 53 years of age during a time discrimination task that required the discrimination of temporal intervals of seconds differing by several hundred milliseconds. Increasing development was associated with progressive activation increases within left lateralized dorsolateral and inferior fronto-parieto-striato-thalamic brain regions. Furthermore, despite comparable task performance, adults showed increased functional connectivity between inferior/dorsolateral interhemispheric fronto-frontal activation as well as between inferior fronto-parietal regions compared with adolescents. Activation in caudate, specifically, was associated with both increasing age and better temporal discrimination. Progressive decreases in activation with age were observed in ventromedial prefrontal cortex, limbic regions, and cerebellum. The findings demonstrate age-dependent developmentally dissociated neural networks for time discrimination. With increasing age there is progressive recruitment of later maturing left hemispheric and lateralized fronto-parieto-striato-thalamic networks, known to mediate time discrimination in adults, while earlier developing brain regions such as ventromedial prefrontal cortex, limbic and paralimbic areas, and cerebellum subserve fine-temporal processing functions in children and adolescents.

[1]  M. Brammer,et al.  Progressive increase of frontostriatal brain activation from childhood to adulthood during event‐related tasks of cognitive control , 2006, Human brain mapping.

[2]  L. Shah,et al.  Functional magnetic resonance imaging. , 2010, Seminars in roentgenology.

[3]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.

[4]  D. V. Cramon,et al.  Subprocesses of Performance Monitoring: A Dissociation of Error Processing and Response Competition Revealed by Event-Related fMRI and ERPs , 2001, NeuroImage.

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

[6]  Gereon R. Fink,et al.  Developmental changes in neural activation and psychophysiological interaction patterns of brain regions associated with interference control and time perception , 2008, NeuroImage.

[7]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[8]  Paul M. Thompson,et al.  Gender differences in the left inferior frontal gyrus in normal children , 2004, NeuroImage.

[9]  A. L. Lin,et al.  Functional magnetic resonance imaging , 2009 .

[10]  D. Gitelman,et al.  The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. , 2008, Cerebral cortex.

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

[12]  T A Carpenter,et al.  Colored noise and computational inference in neurophysiological (fMRI) time series analysis: Resampling methods in time and wavelet domains , 2001, Human brain mapping.

[13]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[14]  N. Minshew,et al.  Maturation of Widely Distributed Brain Function Subserves Cognitive Development , 2001, NeuroImage.

[15]  E. Bullmore,et al.  Methods for diagnosis and treatment of stimulus‐correlated motion in generic brain activation studies using fMRI , 1999, Human brain mapping.

[16]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[17]  V. Menon,et al.  Maturation of brain function associated with response inhibition. , 2002, Journal of the American Academy of Child and Adolescent Psychiatry.

[18]  Gary H. Glover,et al.  A Developmental fMRI Study of the Stroop Color-Word Task , 2002, NeuroImage.

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

[20]  Martin P. Paulus,et al.  Accumulation of neural activity in the posterior insula encodes the passage of time , 2008, Neuropsychologia.

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

[22]  Nathaniel S. Miller,et al.  The time of our lives: life span development of timing and event tracking. , 2006, Journal of experimental psychology. General.

[23]  Wolfgang Grodd,et al.  Discrimination of temporal information at the cerebellum: functional magnetic resonance imaging of nonverbal auditory memory , 2004, NeuroImage.

[24]  Jin Fan,et al.  Development of attentional networks: An fMRI study with children and adults , 2005, NeuroImage.

[25]  M. Brammer,et al.  Linear age‐correlated functional development of right inferior fronto‐striato‐cerebellar networks during response inhibition and anterior cingulate during error‐related processes , 2007, Human brain mapping.

[26]  Stefan Ehrlich,et al.  Influence of age and movement complexity on kinematic hand movement parameters in childhood and adolescence , 2008, International Journal of Developmental Neuroscience.

[27]  Rozmin Halari,et al.  Effects of age and sex on developmental neural networks of visual–spatial attention allocation , 2010, NeuroImage.

[28]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[29]  S Lehéricy,et al.  Basal ganglia and supplementary motor area subtend duration perception: an fMRI study , 2003, NeuroImage.

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

[31]  M. Roesch,et al.  Orbitofrontal cortex, decision-making and drug addiction , 2006, Trends in Neurosciences.

[32]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

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

[34]  Katya Rubia,et al.  Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection , 2003, NeuroImage.

[35]  Laurence Steinberg,et al.  Age differences in future orientation and delay discounting. , 2009, Child development.

[36]  R. Ivry,et al.  Perception and production of temporal intervals across a range of durations: evidence for a common timing mechanism. , 1995, Journal of experimental psychology. Human perception and performance.

[37]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[38]  B. Ardekani,et al.  Functional magnetic resonance imaging of brain activity in the visual oddball task. , 2002, Brain research. Cognitive brain research.

[39]  Massimo Volpe,et al.  Hemodynamic Responses , 2005 .

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

[41]  Peter A. Hancock,et al.  Developmental Changes in Human Duration Judgments: A Meta-Analytic Review , 1999 .

[42]  R. Joseph Environmental Influences on Neural Plasticity, the Limbic System, Emotional Development and Attachment: A Review , 1999, Child psychiatry and human development.

[43]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[44]  Benjamin Morillon,et al.  Three Stages and Four Neural Systems in Time Estimation , 2009, The Journal of Neuroscience.

[45]  E. C. Ritchie,et al.  Gender Differences , 1981, Language in Society.

[46]  Ernst Pöppel,et al.  Duration processing in children as determined by time reproduction: implications for a few seconds temporal window. , 2002, Acta psychologica.

[47]  W. Meck,et al.  Neuroanatomical and Neurochemical Substrates of Timing , 2011, Neuropsychopharmacology.

[48]  Fernando Zelaya,et al.  Distinct roles of prefrontal cortical subregions in the Iowa Gambling Task. , 2009, Cerebral cortex.

[49]  Vince D. Calhoun,et al.  Functional neural networks underlying response inhibition in adolescents and adults , 2007, Behavioural Brain Research.

[50]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[51]  J Nuyts,et al.  Different perceptual tasks performed with the same visual stimulus attribute activate different regions of the human brain: a positron emission tomography study. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[52]  C. B. Pedersen,et al.  Cortical Centres Underlying Auditory Temporal Processing in Humans: A PET Study , 2000, Audiology : official organ of the International Society of Audiology.

[53]  Mark A Elliott,et al.  Hemodynamic responses in neural circuitries for detection of visual target and novelty: An event‐related fMRI study , 2007, Human brain mapping.

[54]  S. Keele,et al.  Do perception and motor production share common timing mechanisms: a correctional analysis. , 1985, Acta psychologica.

[55]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

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

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

[58]  R. Benson,et al.  Responses to rare visual target and distractor stimuli using event-related fMRI. , 2000, Journal of neurophysiology.

[59]  Mick Brammer,et al.  Sex-dependent age modulation of frontostriatal and temporo-parietal activation during cognitive control , 2009, NeuroImage.

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

[61]  Sylvie Droit-Volet,et al.  Attentional distraction and time perception in children , 2002 .

[62]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[63]  Florian Klapproth Timing the Future. The Case for a Time-Based Prospective Memory , 2008 .

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

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

[66]  A. Nobre,et al.  Heterogeneity of Cingulate Contributions to Spatial Attention , 2001, NeuroImage.

[67]  Richard B. Ivry,et al.  The cognitive neuropsychology of the cerebellum , 2001 .

[68]  Michael J. Brammer,et al.  Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting , 2011, NeuroImage.

[69]  K. Rubia The Neural Correlates of Timing Functions , 2006 .

[70]  B. Gorman,et al.  Temporal Span and Delay of Gratification as a Function of Age and Cognitive Development , 1977 .

[71]  F. Binkofski,et al.  Cerebral correlates of working memory for temporal information , 2000, NeuroReport.

[72]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[73]  A. L. Greene Future-time perspective in adolescence: The present of things future revisited , 1986, Journal of youth and adolescence.

[74]  S Hale,et al.  A global developmental trend in cognitive processing speed. , 1990, Child development.

[75]  A. Simmons,et al.  Quality Control for Functional MRI Using Automated Data Analysis and Shewhart Charting , 1998, NeuroImage.

[76]  N. Ramnani,et al.  Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition , 2004, Biological Psychiatry.

[77]  Edward J. Sabin,et al.  Development of temporal patterning and vocal hesitations in spontaneous narratives , 1975 .

[78]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[79]  James R. Booth,et al.  Neural development of selective attention and response inhibition , 2003, NeuroImage.

[80]  P. Dawes,et al.  Maturation of visual and auditory temporal processing in school-aged children. , 2008, Journal of speech, language, and hearing research : JSLHR.

[81]  Felipe M. Ortuño,et al.  Sustained attention in a counting task: Normal performance and functional neuroanatomy , 2001, NeuroImage.

[82]  V. Braitenberg Is the cerebellar cortex a biological clock in the millisecond range? , 1967, Progress in brain research.

[83]  Jason R. Tregellas,et al.  Effect of task difficulty on the functional anatomy of temporal processing , 2006, NeuroImage.

[84]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[85]  Hongtu Zhu,et al.  A developmental fMRI study of self‐regulatory control , 2006, Human brain mapping.

[86]  Hui Zhang,et al.  Cluster mass inference via random field theory , 2009, NeuroImage.

[87]  J H Wearden,et al.  Temporal bisection in children. , 2001, Journal of experimental child psychology.

[88]  J. Seamans,et al.  Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay , 1997, The Journal of Neuroscience.

[89]  Michael J. Brammer,et al.  Developmental effects of reward on sustained attention networks , 2011, NeuroImage.

[90]  C. Drake,et al.  The development of rhythmic attending in auditory sequences: attunement, referent period, focal attending , 2000, Cognition.

[91]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[92]  M. Brammer,et al.  Right Ventromedial and Dorsolateral Prefrontal Cortices Mediate Adaptive Decisions under Ambiguity by Integrating Choice Utility and Outcome Evaluation , 2009, The Journal of Neuroscience.

[93]  On the development of low-level auditory discrimination and deficits in dyslexia. , 2004, Dyslexia.

[94]  S. Grondin Timing and time perception: A review of recent behavioral and neuroscience findings and theoretical directions , 2010, Attention, perception & psychophysics.

[95]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[96]  E. Bullmore,et al.  Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI , 2000, Neuroscience & Biobehavioral Reviews.

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

[98]  Franck Vidal,et al.  The supplementary motor area in motor and perceptual time processing: fMRI studies , 2006, Cognitive Processing.

[99]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[100]  Katya Rubia,et al.  The neural correlates of cognitive time management: a review. , 2004, Acta neurobiologiae experimentalis.

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

[102]  K. Kiehl,et al.  An event-related fMRI study of visual and auditory oddball tasks , 2001 .

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

[104]  Jen-Chuen Hsieh,et al.  Common neural mechanisms for explicit timing in the sub-second range , 2009, Neuroreport.

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