Abstract
The neural bases of timing mechanisms in the second-to-minute range are currently investigated using multidisciplinary approaches. This paper documents the involvement of the supplementary motor area (SMA) in the encoding of target durations by reporting convergent fMRI data from motor and perceptual timing tasks. Event-related fMRI was used in two temporal procedures, involving (1) the production of an accurate interval as compared to an accurate force, and (2) a dual-task of time and colour discrimination with parametric manipulation of the level of attention attributed to each parameter. The first study revealed greater activation of the SMA proper in skilful control of time compared to force. The second showed that increasing attentional allocation to time increased activity in a cortico-striatal network including the pre-SMA (in contrast with the occipital cortex for increasing attention to colour). Further, the SMA proper was sensitive to the attentional modulation cued prior to the time processing period. Taken together, these data and related literature suggest that the SMA plays a key role in time processing as part of the striato-cortical pathway previously identified by animal studies, human neuropsychology and neuroimaging.
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Ackermann H, Gräber S, Hertrich I, Daum I (1999) Cerebellar contributions to the perception of temporal cues within the speech and nonspeech domain. Brain Lang 67:228–241
Basso G, Nichelli P, Wharton CM, Peterson M, Grafman J (2003) Distributed neural systems for temporal production: a functional MRI study. Brain Res Bull 59(5):405–411
Brown SW (1997) Attentional resources in timing: interference effects in concurrent temporal and nontemporal working memory tasks. Percept Psychoph 59:1118–1140
Brunia CHM, de Jong BM, van den Berg-Lenssen MMC, Paans AMJ (2000) Visual feedback about time estimation is related to a right hemisphere activation measured by PET. Exp Brain Res 130:328–337
Casini L, Macar F (1997) Effects of attention manipulation on perceived duration and intensity in the visual modality. Mem Cogn 2:912–818
Cesara A, Hagberg GE, Bianciardi M, Sabatini U (2005) Visually cued motor synchronization: modulation of fMRI activation patterns by baseline condition. Neurosci Lett 373:323–337
Coull J (2004) fMRI studies of temporal attention: allocating attention within, or towards, time. Cogn Brain Res 21:216–226
Coull JT, Vidal F, Nazarian B, Macar F (2004) Functional anatomy of the attentional modulation of time estimation. Science 303(5663):1506–1508
Dettmers C, Fink GR, Lemon RN, Stephan KM, Passingham RE, Silbersweig D, Holmes A, Ridding MC, Brooks DJ, Frackowiak RSJ (1995) Relation between cerebral activity and force in the motor areas of the human brain. J Neurophysiol 74:802–815
Elsinger CL, Rao SM, Zimbelman JL, Reynolds NC, Blindauer KA, Hoffmann RG (2003) Neural basis for impaired time reproduction in Parkinson’s disease: an fMRI study. J Int Neuropsy Soc 9:1088–1098
Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Map 2:189
Friston KJ, Fletcher PC, Josephs O, Holmes AP, Rugg MD, Turner R (1998) Event-related fMRI: characterizing differential responses. NeuroImage 7:30
Gibbon J, Malapani C, Dale CL, Gallistel CR (1997) Toward a neurobiology of temporal cognition: advances and challenges. Curr Opin Neurobiol 7:170–184
Hadjikhani N, Liu AK, Dale AM, Cavanagh P, Tootell RBH (1998) Retinotopy and color sensitivity in human visual cortical area V8. Nat Neurosci 1:235–241
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 116:243–246
Harrington DL, Haaland KY (1999) Neural underpinnings of temporal processing: a review of focal lesion, pharmacological, and functional imaging research. Rev Neurosci 10:91–116
Harrington DL, Boyd LA, Mayer AR, Sheltraw DM, Lee RR, Huang M, Rao SM (2004) Neural representation of interval encoding and decision making. Cogn Brain Res 21:193–205
Hinton SC, Meck WH (2004) Fronto-striatal circuitry activated by human peak-interval timing in the supra-seconds range. Cogn Brain Res 21:171–182
Hinton SC, Harrington DL, Binder JR, Durgerian S, Rao SM (2004) Neural systems supporting timing and chronometric counting: an fMRI study. Cogn Brain Res 21:183–192
Ivry RB, Spencer RMC (2004) The neural representation of time. Curr Opin Neurobiol 14:225–232
Jäncke L, Shah NJ, Peters M (2000) Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. Cogn Brain Res 10:177–183
Jantzen KJ, Steinberg FL, Kelso JAS (2002) Practice-dependent modulation of neural activity during human sensorimotor coordination: a functional magnetic resonance imaging study. Neurosci Lett 332:205–209
Josephs O, Turner R, Friston KJ (1997) Event-related fMRI. Hum Brain Mapping 5:243
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 83:1079–1087
Kudo K, Miyazaki M, Kimura T, Yamanaka K, Kadota H, Hirashima M, Nakajima Y, Nakazawa K, Ohtsuki T (2004) Selective activation and deactivation of the human brain structures between speeded and precisely timed tapping responses to identical visual stimulus: an fMRI study. NeuroImage 22:1291–1301
Kuhtz-Buschbeck JP, Ehrsson HH, Forssberg H (2001) Human brain activity in the control of fine static precision grip forces: an fMRI study. Eur J Neurosci 14:382–390
Lang W, Obrig H, Lindinger G, Cheyne D, Deecke L (1990) Supplementary motor area activation while tapping bimanually different rhythms in musicians. Exp Brain Res 79:504–514
Lewis PA, Miall RC (2003a) Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr Opin Neurobiol 13:1–6
Lewis PA, Miall RC (2003b) Brain activation patterns during measurement of sub-and supra-second intervals. Neuropsychologia 41:1583–1592
Lewis PA, Wing AM, Pope PA, Praamstra P, Miall RC (2004) Brain activity correlates differentially with increasing temporal complexity of rhythms during initialisation, synchronization, and continuation phases of paced finger tapping. Neuropsychologia 42:1301–1312
Macar F, Vidal F (2004) Event-related potentials as indices of time processing: a review. J Psychophysiol 18(2–3):89–104
Macar F, Grondin S, Casini L (1994) Controlled attention sharing influences time estimation. Mem Cogn 22(6):673–686
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 142:539–550
Macar F, Anton J-L, Bonnet M, Vidal F (2004) Timing functions of the supplementary motor area: an event-related fMRI study. Cogn Brain Res 21(2):206–215
Mathiak K, Hertrich I, Grodd W, Ackermann H (2004) Discrimination of temporal information at the cerebellum: functional magnetic resonance imaging of nonverbal auditory memory. NeuroImage 21:154–162
Mayville JM, Jantzen KJ, Fuchs A, Steinberg FL, Kelso JAS (2002) Cortical and subcortical networks underlying syncopated and synchronized coordination revealed using fMRI. Hum Brain Mapping 17(4):214–229
Meck WM (1996) Neuropharmacology of timing and time perception. Cogn Brain Res 3:227–242
Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cerebr Cortex 6:342–353
Rao SM, Harrington DL, Haaland KY, Bobholz JA, Cox RW, Binder JR (1997) Distributed neural systems underlying the timing of movements. J Neurosci 17:5528–5535
Rao SM, Mayer AR, Harrington DL (2001) The evolution of brain activation during temporal processing. Nat Neurosci 4:317–323
Rubia K, Overmeyer S, Taylor E, Brammer M, Williams S, Simmons A, Andrew C, Bullmore E (1998) Prefrontal involvement in “temporal bridging” and timing movement. Neuropsychologia 36:1283–1293
Sergent J, Zuck E, Terriah S, MacDonald B (1992) Distributed neural network underlying musical sight-reading and keyboard performance. Science 257:106–109
Smith A, Taylor E, Lidzba K, Rubia K (2003) A right hemispheric frontocerebellar network for time discrimination of several hundreds of milliseconds. NeuroImage 20:344–350
Tanji J (1994) The supplementary motor area in the cerebral cortex. Neurosci Res 19:251–268
Thomas EAC, Weaver WB (1975) Cognitive processing and time perception. Percept Psychoph 17:363–367
Zakay D (1989) Subjective time and attentional resource allocation. An integrated model of time estimation. In: Levin I, Zakay D (eds) Time and human cognition: a life span perspective. North Holland, Amsterdam, pp 365–397
Zeki S, Watson JD, Lueck CJ, Friston KJ, Kennard C, Frackowiak RS (1991) A direct demonstration of functional specialization in human visual cortex. J Neurosci 11:641–649
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Macar, F., Coull, J. & Vidal, F. The supplementary motor area in motor and perceptual time processing: fMRI studies. Cogn Process 7, 89–94 (2006). https://doi.org/10.1007/s10339-005-0025-7
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DOI: https://doi.org/10.1007/s10339-005-0025-7