Dissociation between numerosity and duration processing in aging and early Parkinson's disease

Numerosity and duration processing have been shown to be underlain by a single representational mechanism, namely an accumulator, and to rely on a common cerebral network located principally in areas around the right intraparietal sulcus. However, recent neuropsychological findings reveal a dissociation between numerosity and duration processing, which suggests the existence of partially distinct mechanisms. In this study, we tested the idea of partially common and distinct mechanisms by investigating, for the first time, both numerical and temporal processing abilities in non-demented Parkinson's disease (PD) patients known to suffer from duration impairment and in healthy elderly adults known to have impaired performance in duration tasks. The aim was to assess whether this impaired duration processing would extend to numerosity processing. The participants had to compare either the numerosity of flashed dot sequences or the duration of single dot displays. The results demonstrate an effect of aging on duration comparison, healthy elderly participants making significantly more errors than healthy young participants. Importantly, the performance of PD patients on the duration task was worse than that of the healthy young and elderly groups, whereas no difference was found for numerosity comparison. This dissociation supports the idea that partly independent systems underlie the processing of numerosity and duration.

[1]  Marjan Jahanshahi,et al.  Basal ganglia, dopamine and temporal processing: Performance on three timing tasks on and off medication in Parkinson’s disease , 2008, Brain and Cognition.

[2]  Derrick G. Watson,et al.  Aging and enumeration: a selective deficit for the subitization of targets among distractors. , 2002, Psychology and aging.

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

[4]  Viviane Pouthas,et al.  Effects of internal clock and memory disorders on duration reproductions and duration productions in patients with Parkinson’s disease , 2005, Brain and Cognition.

[5]  F. Yasuno,et al.  Age-related decline of dopamine synthesis in the living human brain measured by positron emission tomography with l-[β-11C]DOPA , 2006 .

[6]  P. Lemaire,et al.  Aging and Mental Arithmetic , 2004 .

[7]  Stephen M. Rao,et al.  Neural basis for impaired time reproduction in Parkinson's disease: An fMRI study , 2003, Journal of the International Neuropsychological Society.

[8]  Paul B. Buckley,et al.  Comparisons of digits and dot patterns. , 1974, Journal of experimental psychology.

[9]  Roger W. Li,et al.  Aging and Visual Counting , 2010, PLoS ONE.

[10]  Marinella Cappelletti,et al.  Dissociations and interactions between time, numerosity and space processing , 2009, Neuropsychologia.

[11]  Warren H. Meck,et al.  Modality differences in timing and temporal memory throughout the lifespan , 2011, Brain and Cognition.

[12]  M. Otsuki,et al.  Deficits of working memory during mental calculation in patients with Parkinson's disease , 2003, Journal of the Neurological Sciences.

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

[14]  Michel Isingrini,et al.  Differential involvement of internal clock and working memory in the production and reproduction of duration: a study on older adults. , 2006, Acta psychologica.

[15]  Patrick Lemaire,et al.  Older and younger adults' strategies in approximate quantification. , 2008, Acta psychologica.

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

[17]  ROBERT S. MOYER,et al.  Time required for Judgements of Numerical Inequality , 1967, Nature.

[18]  A. Nieoullon Dopamine and the regulation of cognition and attention , 2002, Progress in Neurobiology.

[19]  Monica Luciana,et al.  Interval timing and Parkinson’s disease: heterogeneity in temporal performance , 2007, Experimental Brain Research.

[20]  Sylvie Droit-Volet,et al.  Speeding up a master clock common to time, number and length? , 2010, Behavioural Processes.

[21]  Valérie Dormal,et al.  Processing numerosity, length and duration in a three-dimensional Stroop-like task: towards a gradient of processing automaticity? , 2013, Psychological research.

[22]  B. Michel,et al.  Approximate quantification in young, healthy older adults’, and Alzheimer patients , 2009, Brain and Cognition.

[23]  L. Lopiano,et al.  Dissociation between time reproduction of actions and of intervals in patients with Parkinson’s disease , 2010, Journal of Neurology.

[24]  David Abernethy,et al.  The effect of Parkinson’s disease on time estimation as a function of stimulus duration range and modality , 2007, Brain and Cognition.

[25]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[26]  J. Hindle,et al.  Ageing, neurodegeneration and Parkinson's disease. , 2010, Age and ageing.

[27]  R. Church,et al.  A mode control model of counting and timing processes. , 1983, Journal of experimental psychology. Animal behavior processes.

[28]  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.

[29]  Sylvie Droit-Volet,et al.  Relationships Between Age-Related Changes in Time Estimation and Age-Related Changes in Processing Speed, Attention, and Memory , 2002 .

[30]  H. Mehdorn,et al.  Strategy instruction in Parkinson's disease: Influence on cognitive performance , 2010, Neuropsychologia.

[31]  Derrick G. Watson,et al.  Search, enumeration, and aging: eye movement requirements cause age-equivalent performance in enumeration but not in search tasks. , 2005, Psychology and aging.

[32]  L. Nyberg,et al.  The correlative triad among aging, dopamine, and cognition: Current status and future prospects , 2006, Neuroscience & Biobehavioral Reviews.

[33]  M. Falkenstein,et al.  Time estimation in healthy ageing and neurodegenerative basal ganglia disorders , 2008, Neuroscience Letters.

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

[35]  Simon Grondin,et al.  When to start explicit counting in a time-intervals discrimination task: A critical point in the timing process of humans. , 1999 .

[36]  E. Tolosa,et al.  Diagnostic procedures for Parkinson's disease dementia: Recommendations from the movement disorder society task force , 2007, Movement disorders : official journal of the Movement Disorder Society.

[37]  Elena Miró,et al.  Age-related changes and gender differences in time estimation. , 2003, Acta psychologica.

[38]  M. Bondi,et al.  Contributions of frontal system dysfunction to memory and perceptual abilities in Parkinson's disease. , 1993 .

[39]  W. Poewe,et al.  Parkinson's disease and arithmetics: The role of executive functions , 2006, Journal of the Neurological Sciences.

[40]  J. Dalrymple-Alford,et al.  Timing ability and numerical competence in rats. , 1998, Journal of experimental psychology. Animal behavior processes.

[41]  Warren H. Meck,et al.  Chronic treatment with haloperidol induces deficits in working memory and feedback effects of interval timing , 2005, Brain and Cognition.

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

[43]  Emanuele Lo Gerfo,et al.  Impaired reproduction of second but not millisecond time intervals in Parkinson's disease , 2008, Neuropsychologia.

[44]  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.

[45]  D. Geary,et al.  Numerical cognition: age-related differences in the speed of executing biologically primary and biologically secondary processes. , 1998, Experimental aging research.

[46]  Vincent Walsh A theory of magnitude: common cortical metrics of time, space and quantity , 2003, Trends in Cognitive Sciences.

[47]  E. Tolosa,et al.  Brain structural MRI correlates of cognitive dysfunctions in Parkinson's disease , 2011, Journal of the Neurological Sciences.

[48]  Yaakov Stern,et al.  The effects of aging on time reproduction in delayed free-recall , 2005, Brain and Cognition.

[49]  F. Yasuno,et al.  Age-related decline of dopamine synthesis in the living human brain measured by positron emission tomography with L-[beta-11C]DOPA. , 2006, Life sciences.

[50]  P. Lemaire,et al.  Aging and numerosity estimation. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[51]  J. Enns,et al.  Life Span Changes in Visual Enumeration: The Number Discrimination Task , 1996 .

[52]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[53]  M. Sliwinski,et al.  Aging and counting speed: evidence for process-specific slowing. , 1997, Psychology and aging.

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

[55]  F. Craik,et al.  Aging and judgments of duration: Effects of task complexity and method of estimation , 1999, Perception & psychophysics.

[56]  R. Buckner Memory and Executive Function in Aging and AD Multiple Factors that Cause Decline and Reserve Factors that Compensate , 2004, Neuron.

[57]  Michael Andres,et al.  Dissociation of numerosity and duration processing in the left intraparietal sulcus: A transcranial magnetic stimulation study , 2008, Cortex.

[58]  Marinella Cappelletti,et al.  Numbers and time doubly dissociate , 2011, Neuropsychologia.

[59]  Armin Schnider,et al.  Time estimation in Parkinson's disease: normal long duration estimation despite impaired short duration discrimination , 2001, Journal of Neurology.

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

[61]  John Gibbon,et al.  Separating Storage from Retrieval Dysfunction of Temporal Memory in Parkinson's Disease , 2002, Journal of Cognitive Neuroscience.

[62]  V. Walsh,et al.  The parietal cortex and the representation of time, space, number and other magnitudes , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[63]  B. Michel,et al.  Strategic aspects of young, healthy older adults', and Alzheimer patients' arithmetic performance , 2008, Cortex.

[64]  Valérie Dormal,et al.  A common right fronto‐parietal network for numerosity and duration processing: An fMRI study , 2012, Human brain mapping.

[65]  Timing ability and numerical competence in rats. , 1998, Journal of experimental psychology. Animal behavior processes.

[66]  Valérie Dormal,et al.  Processing magnitudes within the parietal cortex , 2012 .

[67]  M. Pesenti,et al.  Numerosity-duration interference: a Stroop experiment. , 2006, Acta psychologica.

[68]  Roi Cohen Kadosh,et al.  Are numbers special? An overview of chronometric, neuroimaging, developmental and comparative studies of magnitude representation , 2008, Progress in Neurobiology.

[69]  V Pouthas,et al.  Timing in aging: the role of attention. , 1999, Experimental aging research.

[70]  Frank Domahs,et al.  Number processing and basal ganglia dysfunction: a single case study , 2004, Neuropsychologia.

[71]  Y. Stern,et al.  Evidence for Age-related Changes to Temporal Attention and Memory from the Choice Time Production Task , 2009, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.