Processing of temporal information and the basal ganglia: new evidence from fMRI

Abstract. Temporal information processing is a fundamental brain function, which might include central timekeeping mechanisms independent of sensory modality. Psychopharmacological and patient studies suggest a crucial role of the basal ganglia in time estimation. In this study, functional magnetic resonance imaging (fMRI) was applied in 15 healthy right-handed male subjects performing an auditory time estimation task (duration discrimination of tone pairs in the range of 1,000–1,400 ms) and frequency discriminations (tone pairs differing in pitch, around 1,000 Hz) as an active control task. Task difficulty was constantly modulated by an adaptive algorithm (weighted up-down method) reacting on individual performance. Time estimation (vs rest condition) elicited a distinct pattern of cerebral activity, including the right medial and both left and right dorsolateral prefrontal cortices (DLPFC), thalamus, basal ganglia (caudate nucleus and putamen), left anterior cingulate cortex, and superior temporal auditory areas. Most activations showed lateralisation to the right hemisphere and were similar in the frequency discrimination task. Comparing time and frequency tasks, we isolated activation in the right putamen restricted to time estimation only. This result supports the notion of central processing of temporal information associated with basal ganglia activity. Temporal information processing in the brain might thus be a distributed process of interaction between modality-dependent sensory cortical function, the putamen (with a timing-specific function), and additional prefrontal cortical systems related to attention and memory. Further investigations are needed to delineate the differential contributions of the striatum and other areas to timing.

[1]  T. Rammsayer,et al.  Are there dissociable roles of the mesostriatal and mesolimbocortical dopamine systems on temporal information processing in humans? , 1997, Neuropsychobiology.

[2]  Thomas Rammsayer,et al.  An experimental comparison of the weighted up-down method and the transformed up-down method , 1992 .

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

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

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

[6]  D R Medoff,et al.  Cerebral blood flow relationships associated with a difficult tone recognition task in trained normal volunteers. , 1998, Cerebral cortex.

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

[8]  J. Gibbon,et al.  Annals of the New York Academy of Sciences. Volume 423. Timing and Time Perception Held at New York on 10-13 May 1983, , 1984 .

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

[10]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[11]  J. Grafman,et al.  Precision and accuracy of subjective time estimation in different memory disorders. , 1993, Brain research. Cognitive brain research.

[12]  Alan C. Evans,et al.  Neural mechanisms underlying melodic perception and memory for pitch , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[14]  J. Desmond,et al.  Load-Dependent Roles of Frontal Brain Regions in the Maintenance of Working Memory , 1999, NeuroImage.

[15]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[16]  W. Kaiser,et al.  Challenging the anterior attentional system with a continuous performance task: a functional magnetic resonance imaging approach , 1998, European Archives of Psychiatry and Clinical Neuroscience.

[17]  M. Petrides,et al.  Functional Organization of the Human Frontal Cortex for Mnemonic Processing. , 1995, Annals of the New York Academy of Sciences.

[18]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[19]  G. B. Wetherill,et al.  Sequential estimation of quantal response curves: A new method of estimation , 1966 .

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

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

[22]  Juha Rinne,et al.  Tone duration discrimination in Parkinson's disease , 1997, Neuropsychologia.

[23]  H. Sauer,et al.  Brain activation during cognitive stimulation with the Wisconsin card sorting test—A functional MRI study on healthy volunteers and schizophrenics , 1998, Schizophrenia Research.

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

[25]  Adrian M. Owen,et al.  The role of the lateral frontal cortex in mnemonic processing: the contribution of functional neuroimaging , 2000, Experimental Brain Research.

[26]  Raymond P. Kesner,et al.  Memory for Duration: Role of Hippocampus and Medial Prefrontal Cortex , 1998, Neurobiology of Learning and Memory.

[27]  J A Obeso,et al.  Temporal discrimination is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

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

[29]  Richard S. J. Frackowiak,et al.  Analysis of temporal structure in sound by the human brain , 1998, Nature Neuroscience.

[30]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

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

[32]  C Kaernbach,et al.  Simple adaptive testing with the weighted up-down method , 1991, Perception & psychophysics.

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

[34]  J. Gibbon,et al.  Timing and time perception. , 1984, Annals of the New York Academy of Sciences.

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

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

[37]  Edward E. Smith,et al.  A parametric study of prefrontal cortex involvement in human working memory , 1996, NeuroImage.

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

[39]  T. Rammsayer,et al.  Impaired temporal discrimination in Parkinson's disease: temporal processing of brief durations as an indicator of degeneration of dopaminergic neurons in the basal ganglia. , 1997, The International journal of neuroscience.

[40]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[41]  A. Holmes Generalisability, random effects and population inference (abstract) , 1998 .

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

[43]  Paul Fraisse,et al.  Psychologie du temps , 1959 .

[44]  C D Marsden,et al.  Differing patterns of striatal 18F‐dopa uptake in Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy , 1990, Annals of neurology.

[45]  The neuropsychology of human temporal information processing , 1993 .

[46]  E. Friedman,et al.  Temporal processing. , 1991, Journal of learning disabilities.

[47]  T. Rammsayer Effects of body core temperature and brain dopamine activity on timing processes in humans , 1997, Biological Psychology.

[48]  B. Damasceno Time perception as a complex functional system: neuropsychological approach. , 1996, The International journal of neuroscience.

[49]  P. Fraisse The psychology of time , 1963 .

[50]  T. Paus,et al.  Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex: a review of 107 PET activation studies , 1998, Neuroreport.

[51]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[52]  Y Kaneoke,et al.  Multisecond oscillations in firing rate in the basal ganglia: robust modulation by dopamine receptor activation and anesthesia. , 1999, Journal of neurophysiology.