The function of dopaminergic neural signal transmission in auditory pulse perception: Evidence from dopaminergic treatment in Parkinson's patients

Auditory pulse perception, which is the perception of relatively salient and regularly appearing events in an acoustic sequence, is a necessary function in humans and has been suggested to rely on basal ganglia function. Our study investigated the effect dopamine depletion has on the auditory pulse perception in Parkinson's disease (PD). We examined PD patients and healthy seniors in this study, and all participants performed a pulse perception task and a motor control task. The pulse perception task consisted of a two alternative forced choice task in which subjects had to identify stimuli as metrical or non-metrical. We tested PD patients before and after the administration of l-3,4-dihydroxyphenylalanin (l-DOPA). The healthy control group performed the same tasks twice. PD patients that were dopamine depleted performed the pulse perception task equally well and as fast as did the healthy control group. However, after the administration of l-DOPA, PD patients performed the pulse perception task significantly faster than they did before the pharmacological intervention, which showed that pulse perception can be modulated by dopaminergic stimulation. These findings indicate that pulse perception relies on dopaminergic mechanisms but is not affected by dopamine depletion in the early stages of PD.

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

[2]  Peter Essens,et al.  Perception of Temporal Patterns , 1985 .

[3]  R. Parncutt A Perceptual Model of Pulse Salience and Metrical Accent in Musical Rhythms , 1994 .

[4]  L. Demany,et al.  Auditory temporal processing in Parkinson's disease , 2008, Neuropsychologia.

[5]  F. Vidal,et al.  Functional Anatomy of the Attentional Modulation of Time Estimation , 2004, Science.

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

[7]  Ray Jackendoff,et al.  An overview of hierarchical structure in music , 1983 .

[8]  Jeffrey M. Hausdorff,et al.  Rhythmic auditory stimulation modulates gait variability in Parkinson's disease , 2007, The European journal of neuroscience.

[9]  M. Annett,et al.  Five Tests of Hand Skill , 1992, Cortex.

[10]  N. Sawamoto,et al.  Cognitive deficits and striato-frontal dopamine release in Parkinson's disease. , 2008, Brain : a journal of neurology.

[11]  T. Rammsayer,et al.  Neuropharmacological Evidence for Different Timing Mechanisms in Humans , 1999, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[12]  Thomas Rammsayer,et al.  Neuropharmacological Approaches to Human Timing , 2008 .

[13]  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.

[14]  J. Snyder,et al.  Pulse and Meter as Neural Resonance , 2009, Annals of the New York Academy of Sciences.

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

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

[17]  Bruno H. Repp,et al.  Hearing a melody in different ways: Multistability of metrical interpretation, reflected in rate limits of sensorimotor synchronization , 2007, Cognition.

[18]  Jeffrey M. Hausdorff,et al.  Marked alterations in the gait timing and rhythmicity of patients with de novo Parkinson's disease , 2006, The European journal of neuroscience.

[19]  Hans Forssberg,et al.  Listening to rhythms activates motor and premotor cortices , 2009, Cortex.

[20]  Timothy D. Griffiths,et al.  Distinct Neural Substrates of Duration-Based and Beat-Based Auditory Timing , 2011, The Journal of Neuroscience.

[21]  M. Jones,et al.  Temporal Aspects of Stimulus-Driven Attending in Dynamic Arrays , 2002, Psychological science.

[22]  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.

[23]  Warren H Meck,et al.  Frontal-striatal circuitry activated by human peak-interval timing in the supra-seconds range. , 2004, Brain research. Cognitive brain research.

[24]  W. Meck Neuropsychology of timing and time perception , 2005, Brain and Cognition.

[25]  J G Martin,et al.  Rhythmic (hierarchical) versus serial structure in speech and other behavior. , 1972, Psychological review.

[26]  T. Robbins,et al.  Dopaminergic modulation of high-level cognition in Parkinson's disease: the role of the prefrontal cortex revealed by PET. , 2002, Brain : a journal of neurology.

[27]  M. Thaut,et al.  Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson's disease. , 1997, Journal of neurology, neurosurgery, and psychiatry.

[28]  Paul Fraisse,et al.  Les structures rythmiques , 1960 .

[29]  W. Meck,et al.  Habit formation and the loss of control of an internal clock: inverse relationship between the level of baseline training and the clock-speed enhancing effects of methamphetamine , 2007, Psychopharmacology.

[30]  Aniruddh D. Patel,et al.  The influence of metricality and modality on synchronization with a beat , 2005, Experimental Brain Research.

[31]  D J Povel,et al.  Internal representation of simple temporal patterns. , 1981, Journal of experimental psychology. Human perception and performance.

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

[33]  M. Thaut,et al.  Neural Basis of Rhythmic Timing Networks in the Human Brain , 2003, Annals of the New York Academy of Sciences.

[34]  W. Meck Neuroanatomical localization of an internal clock: A functional link between mesolimbic, nigrostriatal, and mesocortical dopaminergic systems , 2006, Brain Research.

[35]  P J Essens,et al.  Hierarchical organization of temporal patterns , 1986, Perception & psychophysics.

[36]  H. Braak,et al.  Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen , 2003, Journal of Neural Transmission.

[37]  Stephen Handel,et al.  The contextual nature of rhythmic interpretation , 1983, Perception & psychophysics.

[38]  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.

[39]  E. Large,et al.  The dynamics of attending: How people track time-varying events. , 1999 .

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

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

[42]  Rosanna Cousins,et al.  Stimulus timing by people with Parkinson’s disease , 2008, Brain and Cognition.

[43]  J. Kelso,et al.  A parametric fMRI investigation of context effects in sensorimotor timing and coordination , 2007, Neuropsychologia.

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

[45]  M. Brett,et al.  Impairment of beat-based rhythm discrimination in Parkinson's disease , 2009, Cortex.

[46]  M D'Esposito,et al.  Enhanced frontal function in Parkinson's disease. , 2010, Brain : a journal of neurology.

[47]  W. Meck,et al.  Neuropsychological mechanisms of interval timing behavior. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[48]  Leonard B. Meyer Emotion and Meaning in Music , 1957 .

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

[50]  M. Jones,et al.  Rhythmic context modulates foreperiod effects , 2010 .

[51]  Wolfgang Staffen,et al.  Stimulating music increases motor coordination in patients afflicted with Morbus Parkinson , 2004, Neuroscience Letters.

[52]  R. Zatorre,et al.  Listening to musical rhythms recruits motor regions of the brain. , 2008, Cerebral cortex.

[53]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[54]  Daniel Sanabria,et al.  Rhythms that speed you up. , 2011, Journal of experimental psychology. Human perception and performance.

[55]  Jeffrey M. Hausdorff,et al.  Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson's disease , 2005, Movement disorders : official journal of the Movement Disorder Society.

[56]  Martin Wiener,et al.  Double Dissociation of Dopamine Genes and Timing in Humans , 2011, Journal of Cognitive Neuroscience.

[57]  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.

[58]  Deborah L. Harrington,et al.  Neurobehavioral Mechanisms of Temporal Processing Deficits in Parkinson's Disease , 2011, PloS one.

[59]  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.

[60]  C. Wright,et al.  Temporal rescaling of simple and complex ratios in rhythmic tapping. , 1995 .

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

[62]  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.

[63]  John H Wearden,et al.  Short Article: Effect of Click Trains on Duration Estimates by People with Parkinson's Disease , 2009, Quarterly journal of experimental psychology.

[64]  A. Graybiel,et al.  The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. , 1999, Brain : a journal of neurology.

[65]  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.

[66]  Jessica A. Grahn,et al.  The role of the basal ganglia in learning and memory: Neuropsychological studies , 2009, Behavioural Brain Research.

[67]  A. Graybiel Neurotransmitters and neuromodulators in the basal ganglia , 1990, Trends in Neurosciences.

[68]  P. Essens,et al.  Metrical and nonmetrical representations of temporal patterns , 1985, Perception & psychophysics.

[69]  Gábor P. Háden,et al.  Newborn infants detect the beat in music , 2009, Proceedings of the National Academy of Sciences.