Skip to main content
SpringerLink
Log in

The role of top-down control in different phases of a sensorimotor timing task: a DCM study of adults and adolescents

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

The ability to precisely coordinate motor control to regularly-paced sensory stimuli requires an ability often called ‘mental timekeeping’, a distinct form of cognitive function. A consistent feature among conceptual models of the internal clock mechanism is an element of ‘top-down’ cognitive control. Although lesion and fMRI studies have provided indirect evidence supporting the role of the prefrontal cortex in exerting top-down influence over lower-level sensory and motor regions, little direct evidence exists. We investigated changes in Dynamic Causal Modeling (DCM)-measured top-down control of sensorimotor timing during different phases of a unimanual, auditory-paced finger-tapping task in a cohort of healthy adults and adolescents. The brain regions examined were organized into a network of excitatory connections between bilateral dorso- and ventrolateral prefrontal cortices and motor and auditory cortices. This baseline connectivity changed depending on whether participants listened passively to the pacing cue, synchronized their regular interval finger tapping with the cue, or continued tapping in absence of the cue. Subjects who performed better at maintaining the prescribed tapping pace in the absence of the auditory cue relied more on top-down control of the motor and sensory regions, while those with less accurate performance relied more on sensory driven, bottom-up control of the motor cortex. No significant maturational effects were observed in either the behavioral or DCM path weight data. Both right and left prefrontal cortex were found to exert control over timing behavioral accuracy, but there were distinctly lateralized roles with respect to optimal performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Buhusi, C. V., & Meck, W. H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nature Reviews Neuroscience, 6(10), 755–765. doi:10.1038/nrn1764.

    Article  PubMed  CAS  Google Scholar 

  • Buxton, R. B., Wong, E. C., & Frank, L. R. (1998). Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magnetic Resonance in Medicine, 39(6), 855–864.

    Article  PubMed  CAS  Google Scholar 

  • Cabeza, R., Locantore, J. K., & Anderson, N. D. (2003). Lateralization of prefrontal activity during episodic memory retrieval: evidence for the production-monitoring hypothesis. Journal of Cognitive Neuroscience, 15(2), 249–259. doi:10.1162/089892903321208187.

    Article  PubMed  Google Scholar 

  • Chadick, J. Z., & Gazzaley, A. (2011). Differential coupling of visual cortex with default or frontal-parietal network based on goals. Nature Neuroscience, 14(7), 830–832. doi:10.1038/nn.2823.

    Article  PubMed  CAS  Google Scholar 

  • Cieslik, E. C., Zilles, K., Grefkes, C., & Eickhoff, S. B. (2011). Dynamic interactions in the fronto-parietal network during a manual stimulus–response compatibility task. NeuroImage, 58(3), 860–869. doi:10.1016/j.neuroimage.2011.05.089.

    Article  PubMed  Google Scholar 

  • Collier, G. L., & Ogden, R. T. (2004). Adding drift to the decomposition of simple isochronous tapping: an extension of the Wing-Kristofferson model. Journal of Experimental Psychology. Human Perception and Performance, 30(5), 853–872. doi:10.1037/0096-1523.30.5.853.

    Article  PubMed  Google Scholar 

  • Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215. doi:10.1038/nrn755.

    Article  PubMed  CAS  Google Scholar 

  • Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18, 193–222. doi:10.1146/annurev.ne.18.030195.001205.

    Article  PubMed  CAS  Google Scholar 

  • Diamond, A., & Goldman-Rakic, P. S. (1989). Comparison of human infants and rhesus monkeys on Piaget’s AB task: evidence for dependence on dorsolateral prefrontal cortex. Experimental Brain Research, 74(1), 24–40.

    Article  CAS  Google Scholar 

  • Duncan, J., Emslie, H., Williams, P., Johnson, R., & Freer, C. (1996). Intelligence and the frontal lobe: the organization of goal-directed behavior. Cognitive Psychology, 30(3), 257–303. doi:10.1006/cogp.1996.0008.

    Article  PubMed  CAS  Google Scholar 

  • Fair, D. A., Dosenbach, N. U., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., et al. (2007). Development of distinct control networks through segregation and integration. Proceedings of the National Academy of Sciences of the United States of America, 104(33), 13507–13512. doi:10.1073/pnas.0705843104.

    Article  PubMed  CAS  Google Scholar 

  • Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U., Church, J. A., Miezin, F. M., et al. (2009). Functional brain networks develop from a “local to distributed” organization. PLoS Computational Biology, 5(5), e1000381. doi:10.1371/journal.pcbi.1000381.

    Article  PubMed  Google Scholar 

  • First, M., Spitzer, R., Gibbon, M., & Williams, J. (1994). Structured clinical interview for Axis I DSM-IV disorders. New York: Biometrics Research.

    Google Scholar 

  • Freire, L., & Mangin, J. F. (2001). Motion correction algorithms may create spurious brain activations in the absence of subject motion. NeuroImage, 14(3), 709–722. doi:10.1006/nimg.2001.0869.

    Article  PubMed  CAS  Google Scholar 

  • Freire, L., Roche, A., & Mangin, J. F. (2002). What is the best similarity measure for motion correction in fMRI time series? IEEE Transactions on Medical Imaging, 21(5), 470–484. doi:10.1109/TMI.2002.1009383.

    Article  PubMed  CAS  Google Scholar 

  • Friston, K. J. (2002). Bayesian estimation of dynamical systems: an application to fMRI. NeuroImage, 16(2), 513–530. doi:10.1006/nimg.2001.1044.

    Article  PubMed  CAS  Google Scholar 

  • Friston, K. J., & Price, C. J. (2001). Generative models, brain function and neuroimaging. Scandinavian Journal of Psychology, 42(3), 167–177.

    Article  PubMed  CAS  Google Scholar 

  • Friston, K. J., Harrison, L., & Penny, W. (2003). Dynamic causal modelling. NeuroImage, 19(4), 1273–1302.

    Article  PubMed  CAS  Google Scholar 

  • Fritz, J. B., Elhilali, M., David, S. V., & Shamma, S. A. (2007). Auditory attention--focusing the searchlight on sound. Current Opinion in Neurobiology, 17(4), 437–455. doi:10.1016/j.conb.2007.07.011.

    Article  PubMed  CAS  Google Scholar 

  • Garavan, H., Ross, T. J., Kaufman, J., & Stein, E. A. (2003). A midline dissociation between error-processing and response-conflict monitoring. NeuroImage, 20(2), 1132–1139. doi:10.1016/S1053-8119(03)00334-3.

    Article  PubMed  CAS  Google Scholar 

  • Garrido, M. I., Kilner, J. M., Kiebel, S. J., Stephan, K. E., & Friston, K. J. (2007). Dynamic causal modelling of evoked potentials: a reproducibility study. NeuroImage, 36(3), 571–580. doi:10.1016/j.neuroimage.2007.03.014.

    Article  PubMed  Google Scholar 

  • Gibbon, J. (1977). Scalar expectancy theory and Weber’s law in animal timing. Psychological Review, 84(3), 279.

    Article  Google Scholar 

  • Greene, L. S., & Williams, H. G. (1993). Age-related differences in timing control of repetitive movement: application of the Wing-Kristofferson model. Research Quarterly for Exercise and Sport, 64(1), 32–38.

    Article  PubMed  CAS  Google Scholar 

  • Guye, M., Bartolomei, F., & Ranjeva, J. P. (2008). Imaging structural and functional connectivity: towards a unified definition of human brain organization? Current Opinion in Neurology, 21(4), 393–403. doi:10.1097/WCO.0b013e3283065cfb.

    Article  PubMed  Google Scholar 

  • Hare, T. A., Schultz, W., Camerer, C. F., O’Doherty, J. P., & Rangel, A. (2011). Transformation of stimulus value signals into motor commands during simple choice. Proceedings of the National Academy of Sciences of the United States of America, 108(44), 18120–18125. doi:10.1073/pnas.1109322108.

    Article  PubMed  CAS  Google Scholar 

  • Jantzen, K. J., Steinberg, F. L., & Kelso, J. A. (2004). Brain networks underlying human timing behavior are influenced by prior context. Proceedings of the National Academy of Sciences of the United States of America, 101(17), 6815–6820. doi:10.1073/pnas.0401300101.

    Article  PubMed  CAS  Google Scholar 

  • Jantzen, K. J., Steinberg, F. L., & Kelso, J. A. (2005). Functional MRI reveals the existence of modality and coordination-dependent timing networks. NeuroImage, 25(4), 1031–1042. doi:10.1016/j.neuroimage.2004.12.029.

    Article  PubMed  CAS  Google Scholar 

  • Jantzen, K. J., Oullier, O., Marshall, M., Steinberg, F. L., & Kelso, J. A. (2007). A parametric fMRI investigation of context effects in sensorimotor timing and coordination. Neuropsychologia, 45(4), 673–684. doi:10.1016/j.neuropsychologia.2006.07.020.

    Article  PubMed  CAS  Google Scholar 

  • Kasess, C. H., Stephan, K. E., Weissenbacher, A., Pezawas, L., Moser, E., & Windischberger, C. (2010). Multi-subject analyses with dynamic causal modeling. NeuroImage, 49(4), 3065–3074. doi:10.1016/j.neuroimage.2009.11.037.

    Article  PubMed  Google Scholar 

  • Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., et al. (1997). Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 980–988. doi:10.1097/00004583-199707000-00021.

    Article  PubMed  CAS  Google Scholar 

  • Knudsen, E. I. (2007). Fundamental components of attention. Annual Review of Neuroscience, 30, 57–78. doi:10.1146/annurev.neuro.30.051606.094256.

    Article  PubMed  CAS  Google Scholar 

  • Lewis, P. A., Wing, A. M., Pope, P. A., Praamstra, P., & Miall, R. C. (2004). Brain activity correlates differentially with increasing temporal complexity of rhythms during initialisation, synchronisation, and continuation phases of paced finger tapping. Neuropsychologia, 42(10), 1301–1312. doi:10.1016/j.neuropsychologia.2004.03.001.

    Article  PubMed  CAS  Google Scholar 

  • Matell, M. S., & Meck, W. H. (2004). Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Brain Research. Cognitive Brain Research, 21(2), 139–170. doi:10.1016/j.cogbrainres.2004.06.012.

    Article  PubMed  Google Scholar 

  • McAuley, J. D., Jones, M. R., Holub, S., Johnston, H. M., & Miller, N. S. (2006). The time of our lives: life span development of timing and event tracking. Journal of Experimental Psychology. General, 135(3), 348–367. doi:10.1037/0096-3445.135.3.348.

    Article  PubMed  Google Scholar 

  • Meck, W. H. (1996). Neuropharmacology of timing and time perception. Brain Research. Cognitive Brain Research, 3(3–4), 227–242.

    Article  PubMed  CAS  Google Scholar 

  • Meck, W. H., & Benson, A. M. (2002). Dissecting the brain’s internal clock: how frontal-striatal circuitry keeps time and shifts attention. Brain and Cognition, 48(1), 195–211. doi:10.1006/brcg.2001.1313.

    Article  PubMed  Google Scholar 

  • Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202. doi:10.1146/annurev.neuro.24.1.167.

    Article  PubMed  CAS  Google Scholar 

  • Molinari, M., Leggio, M. G., & Thaut, M. H. (2007). The cerebellum and neural networks for rhythmic sensorimotor synchronization in the human brain. Cerebellum, 6(1), 18–23. doi:10.1080/14734220601142886.

    Article  PubMed  Google Scholar 

  • Neumann, J., & Lohmann, G. (2003). Bayesian second-level analysis of functional magnetic resonance images. NeuroImage, 20(2), 1346–1355. doi:10.1016/S1053-8119(03)00443-9.

    Article  PubMed  Google Scholar 

  • Opitz, B., Mecklinger, A., & Friederici, A. D. (2000). Functional asymmetry of human prefrontal cortex: encoding and retrieval of verbally and nonverbally coded information. Learning and Memory, 7(2), 85–96.

    Article  PubMed  CAS  Google Scholar 

  • Pollok, B., Gross, J., Muller, K., Aschersleben, G., & Schnitzler, A. (2005). The cerebral oscillatory network associated with auditorily paced finger movements. NeuroImage, 24(3), 646–655. doi:10.1016/j.neuroimage.2004.10.009.

    Article  PubMed  Google Scholar 

  • Rao, S. M., Harrington, D. L., Haaland, K. Y., Bobholz, J. A., Cox, R. W., & Binder, J. R. (1997). Distributed neural systems underlying the timing of movements. Journal of Neuroscience, 17(14), 5528–5535.

    PubMed  CAS  Google Scholar 

  • Rehme, A. K., Eickhoff, S. B., Wang, L. E., Fink, G. R., & Grefkes, C. (2011). Dynamic causal modeling of cortical activity from the acute to the chronic stage after stroke. NeuroImage, 55(3), 1147–1158. doi:10.1016/j.neuroimage.2011.01.014.

    Article  PubMed  Google Scholar 

  • Repp, B. H. (2005). Sensorimotor synchronization: a review of the tapping literature. Psychonomic Bulletin and Review, 12(6), 969–992.

    Article  PubMed  Google Scholar 

  • Rubia, K., & Smith, A. (2004). The neural correlates of cognitive time management: a review. Acta Neurobiologiae Experimentalis (Wars), 64(3), 329–340.

    Google Scholar 

  • Rypma, B., Berger, J. S., & D’Esposito, M. (2002). The influence of working-memory demand and subject performance on prefrontal cortical activity. Journal of Cognitive Neuroscience, 14(5), 721–731. doi:10.1162/08989290260138627.

    Article  PubMed  Google Scholar 

  • Smith, A. B., Giampietro, V., Brammer, M., Halari, R., Simmons, A., & Rubia, K. (2011). Functional development of fronto-striato-parietal networks associated with time perception. Frontiers in Human Neuroscience, 5, 136. doi:10.3389/fnhum.2011.00136.

    Article  PubMed  Google Scholar 

  • Stephan, K. E., Penny, W. D., Moran, R. J., den Ouden, H. E., Daunizeau, J., & Friston, K. J. (2010). Ten simple rules for dynamic causal modeling. NeuroImage, 49(4), 3099–3109. doi:10.1016/j.neuroimage.2009.11.015.

    Article  PubMed  CAS  Google Scholar 

  • Stevens, M. C., Kiehl, K. A., Pearlson, G., & Calhoun, V. D. (2007). Functional neural circuits for mental timekeeping. Human Brain Mapping, 28(5), 394–408. doi:10.1002/hbm.20285.

    Article  PubMed  Google Scholar 

  • Tanji, J., & Hoshi, E. (2008). Role of the lateral prefrontal cortex in executive behavioral control. Physiological Reviews, 88(1), 37–57. doi:10.1152/physrev.00014.2007.

    Article  PubMed  Google Scholar 

  • Teki, S., Grube, M., Kumar, S., & Griffiths, T. D. (2011). Distinct neural substrates of duration-based and beat-based auditory timing. Journal of Neuroscience, 31(10), 3805–3812. doi:10.1523/JNEUROSCI.5561-10.2011.

    Article  PubMed  CAS  Google Scholar 

  • Vendrell, P., Junque, C., Pujol, J., Jurado, M. A., Molet, J., & Grafman, J. (1995). The role of prefrontal regions in the Stroop task. Neuropsychologia, 33(3), 341–352.

    Article  PubMed  CAS  Google Scholar 

  • Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: a meta-analysis. Cognitive, Affective, & Behavioral Neuroscience, 3(4), 255–274.

    Article  Google Scholar 

  • Wencil, E. B., Coslett, H. B., Aguirre, G. K., & Chatterjee, A. (2010). Carving the clock at its component joints: neural bases for interval timing. Journal of Neurophysiology, 104(1), 160–168. doi:10.1152/jn.00029.2009.

    Article  PubMed  Google Scholar 

  • Wiener, M., Turkeltaub, P., & Coslett, H. B. (2010). The image of time: a voxel-wise meta-analysis. NeuroImage, 49(2), 1728–1740. doi:10.1016/j.neuroimage.2009.09.064.

    Article  PubMed  Google Scholar 

  • Wing, A. M. (2002). Voluntary timing and brain function: an information processing approach. Brain and Cognition, 48(1), 7–30. doi:10.1006/brcg.2001.1301.

    Article  PubMed  Google Scholar 

  • Wing, A. M., & Kristofferson, A. (1973). The timing of interresponse intervals. Attention, Perception, & Psychophysics, 13(3), 455–460.

    Article  Google Scholar 

  • Witt, S. T., Laird, A. R., & Meyerand, M. E. (2008). Functional neuroimaging correlates of finger-tapping task variations: an ALE meta-analysis. NeuroImage, 42(1), 343–356. doi:10.1016/j.neuroimage.2008.04.025.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Olin Neuropsychiatry Research Center, Institute of Living, Hartford Hospital, 200 Retreat Avenue, ONRC, Whitehall Building, Hartford, CT, 06106, USA

    Suzanne T. Witt & Michael C. Stevens

  2. Department of Psychiatry, Yale University School of Medicine, 300 George Street, Suite 901, New Haven, CT, 06511, USA

    Michael C. Stevens

Authors
  1. Suzanne T. Witt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael C. Stevens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Suzanne T. Witt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Witt, S.T., Stevens, M.C. The role of top-down control in different phases of a sensorimotor timing task: a DCM study of adults and adolescents. Brain Imaging and Behavior 7, 260–273 (2013). https://doi.org/10.1007/s11682-013-9224-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-013-9224-5

Keywords

Search

Navigation