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01-10-2004 | Research Article

The right dorsolateral prefrontal cortex is essential in time reproduction: an investigation with repetitive transcranial magnetic stimulation

Authors: Catherine R. G. Jones, Karin Rosenkranz, John C. Rothwell, Marjan Jahanshahi

Published in: Experimental Brain Research | Issue 3/2004

Abstract

This study used repetitive transcranial magnetic stimulation (rTMS) to investigate the roles of the right dorsolateral prefrontal cortex (DLPFC) and supplementary motor area (SMA) in short (500 ms) and long (2 s) interval timing. The results were compared with rTMS over the leg area of motor cortex, an area not thought to be involved with time estimation. rTMS was delivered during one of two phases of a time reproduction task: at the onset of the Estimation Phase (presentation of the interval to be timed) and at the onset of the Reproduction Phase (subjects’ reproduction of the timed interval). There was a significant main effect of Site (SMA vs. right DLPFC vs. leg motor area) due to the fact that rTMS over the right DLPFC caused subjects to underestimate time intervals compared with rTMS over the leg motor area. There was also a significant three-way interaction between Site, Duration and Phase (Estimation Phase vs. Reproduction Phase) that post hoc analyses showed was due to underestimation of long intervals when rTMS was given over the right DLPFC at the start of the Reproduction Phase. There was no effect of rTMS over the right DLPFC or SMA in the short interval task. This is consistent with previous studies showing that the right DLPFC is important in estimating time intervals in the seconds-range. In addition, we suggest that the selectivity of the rTMS effect for the Reproduction Phase indicates that the right DLPFC plays a particular role in memory processes.

Alexander GE, Crutcher MD, DeLong MR (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res 85:119–146PubMed

Breukelaar JW, Dalrymple-Alford JC (1999) Effects of lesions to the cerebellar vermis and hemispheres on timing and counting in rats. Behav Neurosci 113:78–90CrossRefPubMed

Brunia CH, de Jong BM, van den Berg-Lenssen MMC, Paans AM (2000) Visual feedback about time estimation is related to a right hemisphere activation measured by PET. Exp Brain Res 130:328–337CrossRefPubMed

Casini L, Ivry RB (1999) Effects of divided attention on temporal processing in patients with lesions of the cerebellum or frontal lobe. Neuropsychology 13:10–21CrossRefPubMed

Clarke S, Ivry RB, Grinband J, Roberts S, Shimizu N (1996) Exploring the domain of the cerebellar timing system. In: Pastor MA, Artieda J (eds) Time, internal clocks, and movement. Elsevier, New York, pp 257–280

Constantinidis C, Williams GV, Goldman-Rakic PS (2002) A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 5:175–180CrossRefPubMed

Damen EJ, Brunia CH (1994) Is a stimulus conveying task-relevant information a sufficient condition to elicit a stimulus-preceding negativity? Psychophysiology 31:129–139PubMed

Epstein CM, Sekino M, Yamaguchi K, Kamiya S, Ueno S (2002) Asymmetries of prefrontal cortex in human episodic memory: effects of transcranial magnetic stimulation on learning abstract patterns. Neurosci Lett 320:5–8CrossRefPubMed

Fletcher PC, Henson RN (2001) Frontal lobes and human memory: insights from functional neuroimaging. Brain 124:849–881CrossRefPubMed

Fortin C, Breton R (1995) Temporal interval production and processing in working memory. Percept Psychophys 57:203–215PubMed

Fortin C, Rousseau R (1998) Interference from short-term memory processing on encoding and reproducing brief durations. Psychol Res 61:269–276CrossRefPubMed

Fortin C, Rousseau R, Bourque P, Kirouac E (1993) Time estimation and concurrent nontemporal processing: specific interference from short-term memory demands. Percept Psychophys 53:536–548PubMed

Gibbon J, Church RM, Meck WH (1984) Scalar timing in memory. Annals of the New York Academy of Sciences Vol 423:52–77

Goldman-Rakic PS (1996) Regional and cellular fractionation of working memory. Proc Natl Acad Sci U S A 93:13473–13480CrossRefPubMed

Halsband U, Ito N, Tanji J, Freund HJ (1993) The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain 116:243–266PubMed

Harrington DL, Haaland KY, Hermanowicz N (1998) Temporal processing in the basal ganglia. Neuropsychology 12:3–12PubMed

Ivry RB (1996) The representation of temporal information in perception and motor control. Curr Opin Neurobiol 6:851–857PubMed

Ivry RB, Keele SW, Diener HC (1988) Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res 73:167–180PubMed

Jahanshahi M, Rothwell J (2000) Transcranial magnetic stimulation studies of cognition: an emerging field. Exp Brain Res 131:1–9PubMed

Jahanshahi M, Profice P, Brown RG, Ridding MC, Dirnberger G, Rothwell JC (1998) The effects of transcranial magnetic stimulation over the dorsolateral prefrontal cortex on suppression of habitual counting during random number generation. Brain 121:1533–4544CrossRefPubMed

Jones C, Jahanshahi M, Dirnberger G, and Frith CD (2000) Estimation of long vs. short intervals: the functional anatomy of time estimation studied with PET. Cognitive Neuroscience Society Annual Meeting 2000:126–127 (abstract)

Jueptner M, Rijntjes M, Weiller C, Faiss JH, Timmann D, Mueller SP, Diener HC (1995) Localization of a cerebellar timing process using PET. Neurology 45:1540–1545PubMed

Jueptner M, Flerich L, Weiller C, Mueller SP, Diener HC (1996) The human cerebellum and temporal information processing—results from a PET experiment. NeuroReport 7:2761–2765PubMed

Kawashima R, Okuda J, Umetsu A, Sugiura M, Inoue K, Suzuki K, Tabuchi M, Tsukiura T, Narayan SL, Nagasaka T, Yanagawa I, Fujii T, Takahashi S, Fukuda H, Yamadori A (2000) Human cerebellum plays an important role in memory-timed finger movement: an fMRI study. J Neurophysiol 83:1079–1087PubMed

Koch G, Olivieri M, Torriero S, Caltagirone C (2003) Underestimation of time perception after repetitive transcranial magnetic stimulation. Neurology 60:1844–1846PubMed

Lewis PA (2002) Finding the timer. Trends in Cognitive Sciences 6:195–196CrossRefPubMed

Lewis PA, Miall RC (2003) Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr Opin Neurobiol 13:250–255CrossRefPubMed

Macar F, Vidal F, Casini L (1999) The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes. Exp Brain Res 125:271–280PubMed

Macar F, Lejeune H, Bonnet M, Ferrara A, Pouthas V, Vidal F, Maquet P (2002) Activation of the supplementary motor area and of attentional networks during temporal processing. Exp Brain Res 142:475–485CrossRefPubMed

Mangels JA, Ivry RB, Shimizu N (1998) Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. Cognitive Brain Research 7:15–39CrossRefPubMed

Maquet P, Lejeune H, Pouthas V, Bonnet M, Casini L, Macar F, Timsit BM, Vidal F, Ferrara A, Degueldre C, Quaglia L, Delfiore G, Luxen A, Woods R, Mazziotta JC, Comar D (1996) Brain activation induced by estimation of duration: a PET study. NeuroImage 3:119–126PubMed

Maricq AV, Church RM (1983) The differential effects of haloperidol and methamphetamine on time estimation in the rat. Psychopharmacology Berl 79:10–15PubMed

Maricq AV, Roberts S, Church RM (1981) Methamphetamine and time estimation. J Exp Psychol Anim Behav Process 7:18–30PubMed

Meck WH (1983) Selective adjustment of the speed of internal clock and memory processes. J Exp Psychol Anim Behav Process 9:171–201PubMed

Meck WH (1986) Affinity for the dopamine D2 receptor predicts neuroleptic potency in decreasing the speed of an internal clock. Pharmacol Biochem Behav 25:1185–1189PubMed

Meck WH, Church RM (1987a) Cholinergic modulation of the content of temporal memory. Behav Neurosci 101:457–464CrossRefPubMed

Meck WH, Church RM (1987b) Nutrients that modify the speed of internal clock and memory storage processes. Behav Neurosci 10:465–475

Michon JA (1985) The compleat time experiencer. In: Michon JA, Jackson JL (eds) Time, mind and behaviour. Springer, Berlin Heidelberg New York, pp 21–52

Mohl W, Pfurtscheller G (1991) The role of the right parietal region in a movement time estimation task. NeuroReport 2:309–312PubMed

Monfort V, Pouthas V, Ragot R (2000) Role of frontal cortex in memory for duration: an event-related potential study in humans. Neurosci Lett 286:91–94CrossRefPubMed

O’Boyle DJ, Freeman JS, Cody FWJ (1996) The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson’s disease. Brain 119:51–70PubMed

Olton DS (1989) Frontal cortex, timing and memory. Neuropsychologia 27:121–130CrossRefPubMed

Pastor MA, Artieda J, Jahanshahi M, Obeso JA (1992a) Time estimation and reproduction is abnormal in Parkinson’s disease. Brain 115:211–225PubMed

Pastor MA, Jahanshahi M, Artieda J, Obeso JA (1992b) Performance of repetitive wrist movements in Parkinson’s disease. Brain 115:875–891PubMed

Penhune VB, Zattore RJ, Evans AC (1998) Cerebellar contributions to motor timing: a PET study of auditory and visual rhythm reproduction. J Cognit Neurosci 10:752–765CrossRef

Penton-Voak IS, Edwards H, Percival A, Wearden JH (1996) Speeding up an internal clock in humans? Effects of click trains on subjective duration. J Exp Psychol Anim Behav Process 22:307–320CrossRefPubMed

Perrett SP (1998) Temporal discrimination in the cerebellar cortex during conditioned eyelid responses. Exp Brain Res 121:115–124CrossRefPubMed

Rammsayer TH (1999) Neuropharmacological evidence for different timing mechanisms in humans. Q J Exp Psychol B 52:273–286CrossRefPubMed

Ramnani N, Passingham RE (2001) Changes in the human brain during rhythm learning. J Cognit Neurosci 13:952–966CrossRef

Rao SM, Harrington DL, Haaland KY, Bobholz JA, Cox RW, Binder JR (1997) Distributed neural systems underlying the timing of movements. J Neurosci 17:5528–5535PubMed

Rao SM, Mayer AR, Harrington DL (2001) The evolution of brain activation during temporal processing. Nat Neurosci. 4:317–323

Schubotz RI, Friederici AD, Von CD (2000) Time perception and motor timing: a common cortical and subcortical basis revealed by fMRI. NeuroImage 11:1–12CrossRefPubMed

Sergent V, Hellige JB, Cherry B (1993) Effects of responding hand and concurrent verbal processing on time-keeping and motor-implementation processes. Brain Cogn 23:243–262CrossRefPubMed

Staddon JER, Higa JJ (1999) Time and memory: towards a pacemaker-free theory of interval timing. J Exp Anal Behavior 71:215–251

Theoret H, Haque J, Pascual-Leone A (2001) Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett 306:29–32CrossRefPubMed

Tracy JI, Faro SH, Mohamed FB, Pinsk M, Pinus A (2000) Functional localization of a “Time Keeper” function separate from attentional resources and task strategy. NeuroImage 11:228–242CrossRefPubMed

Treisman M (1963) Temporal discrimination and the indifference interval: implications for a model of the ‘internal clock’. Psychol Monographs 77:1–31

Wassermann EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5–7, 1996. Electroencephalogr Clin Neurophysiol 108:1–16PubMed

Woodrow H (1951) Time Perception. In: Stevens S (ed) Handbook of experimental psychology. Wiley, New York, pp 1224–1236

Yeo CH, Hardiman MJ, Glickstein M (1985a) Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp Brain Res 60:87–98PubMed

Yeo CH, Hardiman MJ, Glickstein M (1985b) Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60:99–113PubMed

Yeo CH, Hardiman MJ, Glickstein M (1985c) Classical conditioning of the nictitating membrane response of the rabbit. III. Connections of cerebellar lobule HVI. Exp Brain Res 60:114–126PubMed

Zheng XM (2000) Regional cerebral blood flow changes in drug-resistant depressed patients following treatment with transcranial magnetic stimulation: a statistical parametric mapping analysis. Psychiatry Research 100:75–80CrossRefPubMed

Title: The right dorsolateral prefrontal cortex is essential in time reproduction: an investigation with repetitive transcranial magnetic stimulation
Authors: Catherine R. G. Jones
Karin Rosenkranz
John C. Rothwell
Marjan Jahanshahi
Publication date: 01-10-2004
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 3/2004
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-004-1912-3

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The right dorsolateral prefrontal cortex is essential in time reproduction: an investigation with repetitive transcranial magnetic stimulation

Abstract

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