The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.
Both Supplementary and Presupplementary Motor Areas Are Crucial for the Temporal Organization of Multiple Movements
Abstract
Shima, Keisetsu and Jun Tanji. Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J. Neurophysiol. 80: 3247–3260, 1998. To study the involvement of the supplementary (SMA) and presupplementary (pre-SMA) motor areas in performing sequential multiple movements that are individually separated in time, we injected muscimol, a γ-aminobutyric acid agonist, bilaterally into the part of each area that represents the forelimb. Two monkeys were trained to perform three different movements, separated by a waiting time, in four or six different orders. First, each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order, without the visual signals. After the injection of muscimol (3 μl, 5 μg/μl in 10 min) into either the SMA or pre-SMA bilaterally, the animals started making errors in performing the sequence of movements correctly from memory. However, when guided with a visual signal, they could select and perform the three movements correctly. The impaired memory-based sequencing of movements worsened progressively with time until the animals could not perform the task. Yet they still could associate the visual signals with the different movements at that stage. In control experiments on two separate monkeys, we found that injections of the same amount of muscimol into either the SMA or pre-SMA did not cause problems with nonsequential reaching movement regardless of whether it was visually triggered or self-initiated. These results support the view that both the SMA and pre-SMA are crucially involved in sequencing multiple movements over time.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Furthermore, activity in the SMA and pre-SMA increases before voluntary movement, reflecting the preparation to move (21–25).”
From Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. (2007) · cites this paper as [24]
Citations
Cites
Motor Areas of the Medial Wall: A Review of Their Location and Functional Activation
Picard, N., & Strick, P. L. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.3.342 · Cited by 1,712
Supplementary motor area and other cortical areas in organization of voluntary movements in man
Roland, P. E., Larsen, B., Lassen, N. A., & Skinhöj, E. (1980) · Journal of Neurophysiology · doi:10.1152/jn.1980.43.1.118 · Cited by 1,517
Motor sequence learning: a study with positron emission tomography
Jenkins, I., Brooks, D. J., Nixon, P., Frackowiak, R. S. J., & Passingham, R. E. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03775.1994 · Cited by 1,201
Cortical areas and the selection of movement: a study with positron emission tomography
Deiber, M., Passingham, R. E., Colebatch, J. G., Friston, K. J., Nixon, P. D., & Frackowiak, R. S. J. (1991) · Experimental Brain Research · doi:10.1007/bf00231461 · Cited by 895
Neural mechanisms underlying melodic perception and memory for pitch
Zatorre, R. J., Evans, A. C., & Meyer, E. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-04-01908.1994 · Cited by 885
Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey
Luppino, G., Matelli, M., Camarda, R., & Rizzolatti, G. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903380109 · Cited by 795
Functional mapping of sequence learning in normal humans
Grafton, S. T., Hazeltine, E., & Ivry, R. (1995) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1995.7.4.497 · Cited by 720
Role for supplementary motor area cells in planning several movements ahead
Tanji, J., & Shima, K. (1994) · Nature · doi:10.1038/371413a0 · Cited by 683
Self-citationMushiake, H., Inase, M., & Tanji, J. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.3.705 · Cited by 680
Self-citationEvidence for a supplementary eye field
Schlag, J., & Schlag-Rey, M. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.1.179 · Cited by 603
Flagged first, then by citations
Research works printed but not linked: 3
- Miyashita K., 1996, Soc. Neurosci. Abstr., 22, 1862
- Shima K., 1994, Soc. Neurosci. Abstr., 20, 780
- Shima K, 1997, Soc. Neurosci. Abstr., 23, 1553
Cited by
Sorted by citations
Items 201–272 of 272
Neural dynamics of delayed feedback in robot teleoperation: insights from fNIRS analysis
Zhou, T., Ye, Y., Zhu, Q., Vann, W., & Du, J. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1338453 · Cited by 5
Yang, B. T., Miao, R., Tian, Z., Wang, T., Zhu, F., Li, T., Li, W., & Wu, J. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e36736 · Cited by 5
Watanabe, T., Kuwabara, T., Matsumoto, T., Yunoki, K., Horinouchi, T., & Kirimoto, H. (2025) · Cortex · doi:10.1016/j.cortex.2025.03.005 · Cited by 5
Long, Z., Li, R., Wen, X., Jin, Z. H., Chen, K., & Li, Y. (2012) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2012.06.034 · Cited by 6
Roberts, B. R. T., Meade, M. E., & Fernandes, M. A. (2024) · Memory & Cognition · doi:10.3758/s13421-024-01591-y · Cited by 6
Can tasks be inherently boring?
Charney, E. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x13000964 · Cited by 6
Computational Models of Cognitive and Motor Control
Minai, A. A. (2015) · Springer eBooks · doi:10.1007/978-3-662-43505-2_35 · Cited by 5
Mental effort and fatigue as consequences of monotony
Прудков, П. Н. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x13001155 · Cited by 5
The Development of Infants’ Expectations for Event Timing
Comishen, K. J., & Adler, S. A. (2019) · Timing & Time Perception · doi:10.1163/22134468-20191148 · Cited by 5
Volition and the Function of Consciousness
Graves, T., Maniscalco, B., & Lau, H. C. (2010) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195381641.003.0011 · Cited by 5
What’s Next? Sequential Movement Encoding in Primary Motor Cortex
Bremmer, F. (2005) · Neuron · doi:10.1016/j.neuron.2005.03.006 · Cited by 5
Supplementary eye field contributions to the execution of saccades to remembered target locations
Rosenthal, C. R., Hodgson, T. L., Masud Husain, B., & Christopher Kennard, C. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00661-4 · Cited by 5
Exploring the consistent roles of motor areas across voluntary movement and locomotion
Fortier-Lebel, N., & Nakajima, T. (2025) · The Neuroscientist · doi:10.1177/10738584241263758 · Cited by 4
Levy, D. F., Greicius, Q., Wang, C., Ko, E., Xu, D., Andrews, J. P., & Chang, E. F. (2025) · Neurobiology of Language · doi:10.1162/nol_a_00166 · Cited by 4
Martin, A. D., Nassif, J., Chaluvadi, L., Schammel, C. M. G., Newman‐Norlund, R., Bollmann, S., & Absher, J. R. (2024) · NeuroImage Clinical · doi:10.1016/j.nicl.2024.103724 · Cited by 4
Theys, C., Kovacs, S., Peeters, R. R., Melzer, T. R., Wieringen, A. V., & Nil, L. F. D. (2020) · PLoS ONE · doi:10.1371/journal.pone.0228452 · Cited by 4
Volition and the Function of Consciousness
Lau, H. C., & The Society of Christian Philosophers (2009) · Faith and Philosophy · doi:10.5840/faithphil200926554 · Cited by 4
Simon, J. R., Bek, J., Ghanai, K., Bearss, K. A., Barnstaple, R. E., Bar, R. J., & DeSouza, J. F. X. (2023) · doi:10.31234/osf.io/kwy9x · Cited by 4
Lu, Y., Kim, J., & Kim, T. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1178800 · Cited by 3
A software for testing and training visuo-motor coordination for upper limb control
Oliveira, A. S., Andersen, C. Ø., Grimstrup, C. B., Pretzmann, F., Mortensen, N. H., Castro, M. N., & Mrachacz‐Kersting, N. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.06.002 · Cited by 3
Volition and the Function of Consciousness
Lau, H. C. (2009) · The Cognitive Neurosciences · doi:10.7551/mitpress/8029.003.0105 · Cited by 3
The medial frontal cortex, performance monitoring, cognitive control, and decision making
Kirschner, H., & Ullsperger, M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-820480-1.00048-6 · Cited by 4
The Role of Cortical and Subcortical Motor Areas in the Cognitive Control of Movement
Qin-Qin, L. U., Shu-Fen, D. A. I., Kai, G. U., Yang-Fan, Z. U. O., & Yu, P. (2013) · Advances in Psychological Science · doi:10.3724/sp.j.1042.2012.01794 · Cited by 2
The Individual Inclination to an Occupation and its Neuronal Correlate
Gurres, S., Dillmann, K.-U., Reith, W., & Krick, C. M. (2021) · Frontiers in Education · doi:10.3389/feduc.2021.633962 · Cited by 5
Domsch, S., Zapp, J., Schad, L. R., Nees, F., Hill, H., Hermann, D., Mann, K. F., & Vollstädt‐Klein, S. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.10.014 · Cited by 2
Apport de l’analyse spectrale à l’étude de la connectivité cérébrale en IRMf
Fall, S., Lehmann, P., Ambaiki, K., Vallée, J.-N., Meyer, M.-É., & de Marco, G. (2007) · Neurophysiologie Clinique · doi:10.1016/j.neucli.2007.05.003 · Cited by 2
Neurobiological Foundations of Action Planning and Execution
Hommel, B., Brown, S. B. R. E., & Nattkemper, D. (2016) · Springer eBooks · doi:10.1007/978-3-319-09244-7_2 · Cited by 2
Cerebellar Thalamic and Thalamocortical Projections
Sakai, S. T. (2021) · Springer eBooks · doi:10.1007/978-3-030-23810-0_24 · Cited by 2
Real-time brain-machine interface architectures : neural decoding from plan to movement
Shanechi, M. M. (2011) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 2
Decoding higher-order motor information from primate non-primary motor cortices
Nakajima, T., Mushiake, H., Inui, T., & Tanji, J. (2007) · Technology and Health Care · doi:10.3233/thc-2007-15204 · Cited by 2
Self-citationTHE MEDIAL FRONTAL CORTEX, PERFORMANCE MONITORING, COGNITIVE CONTROL, AND DECISION MAKINGPreprint
Kirschner, H., & Ullsperger, M. (2024) · PsyArXiv (OSF Preprints) · doi:10.31234/osf.io/ytrxd · Cited by 2
Neural commonalities and dissociations of human social and experiential learning
Li, T., Wang, L., Zhao, Y., Su, C., Eickhoff, S. B., Olsson, A., Feng, C., & Pan, Y. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106611 · Cited by 1
Raeder, R., Arora, M., Bertocci, M. A., Chase, H. W., Skeba, A. S., Bebko, G. M., Aslam, H. A., Graur, S., Benjamin, O. E., Wang, Y., et al. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03528-0 · Cited by 1
Online planning of sequential actions
Diedrichsen, J., Kashefi, M., Nazerzadeh, A., & Pruszynski, J. A. (2026) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2026.05.006 · Cited by 1
Passingham, R. E. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198844570.003.0003 · Cited by 1
Cognitive control of sequential behavior
de Kleine, E. (2009) · doi:10.3990/1.9789036528375 · Cited by 1
Kimura, M., Matsumoto, N., Ueda, Y., Satoh, T., Minamimoto, T., & Yamada, H. (2002) · Advances in behavioral biology · doi:10.1007/978-1-4757-3538-3_90 · Cited by 1
Lam, T. K. (2016) · TSpace (University of Toronto) · Cited by 1
Kaur, J., & Balasubramaniam, R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.10.544481 · Cited by 1
Li, Y., An, X., Qian, Y., Xu, X. H., Zhao, S., Mohan, H., Bachschmid-Romano, L., Brunel, N., Whishaw, I. Q., & Huang, Z. J. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4624961 · Cited by 1
Weidler, T. (2024) · Research Publications (Maastricht University) · doi:10.26481/dis.20250110tw · Cited by 1
Neurobiologische Grundlagen der Planung und Ausführung von Bewegungen
Hommel, B., & Nattkemper, D. (2011) · Springer-Lehrbuch · doi:10.1007/978-3-642-12858-5_2 · Cited by 1
Lee, W. H., Ku, J. H., Lee, H., Han, K. W., Park, J.-S., Kim, J., Kim, I. Y., & Kim, S. I. (2009) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-540-92841-6_246
Kinoshita, H., Aoki, T., Tsuda, H., Oku, N., & Hashikawa, K. (2002) · Biomechanisms · doi:10.3951/biomechanisms.16.101
The Function of Consciousness in Controlling Behavior
Steele, S., & Lau, H. C. (2013) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199988341.003.0019
Modularity analysis of brain network under real-time working memory feedback training
Yu, X., & Zhao, X. (2016) · International Joint Conference on Neural Networks (IJCNN) · doi:10.1109/ijcnn.2016.7727807
Legon, W. (2009) · UWSpace (University of Waterloo)
The Neuroimaging of Vicarious Pain
Terrighena, E. L., & Lee, T. M. C. (2017) · Springer eBooks · doi:10.1007/978-3-319-48046-6_16 · Cited by 1
Entrainment and maintenance of an internal metronome in premotor cortexPreprint
Cadena-Valencia, J., García‐Garibay, O., Merchant, H., Jazayeri, M., & de Lafuente, V. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/394783
How the brain controls hand actions : TMS, fMRI and behavioural studies
Tonin, D. (2018) · UEA Digital Repository (University of East Anglia)
Baker, K. M. (2017) · Libraries and Cultural Resources (University of Calgary) · doi:10.11575/prism/26829
Feature Integration in Motor Sequences: Implications for Abstract Task Sequence Studies
Doyle, H. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0638-23.2023
Brain Activation of Motor Imagery and Execution in Latin Dance: Evidence from fNIRSPreprint
Zhang, J., Tan, X., Hu, M., & Song, Y. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4678164
Yinshuang, S. H. I., Menghuan, W. A. N. G., Pan, Y., & Feng, L. I. N. (2024) · Rehabilitation Medicine · doi:10.3724/sp.j.1329.2024.03008
Gradual consolidation of skilled sequential movements in primary motor cortex of non-human primatesPreprint
Ohbayashi, M., & Picard, N. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.06.616850
Differential motor neuron activity in rats during successful and failed grasping
Viaro, R., Bernardi, D., Maggiolini, E., D’Ausilio, A., Ferroni, C. G., Parmiani, P., & Fadiga, L. (2025) · Cerebral Cortex · doi:10.1093/cercor/bhaf032
Tang, S., Qin, B., Zhang, Y., Wei, Y., Liang, J., Liang, J., & Liang, Z. (2025) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2025.1682584
Revealing neural representations of movements and skill using multi voxel pattern analysis
Wiestler, T. (2012) · UCL Discovery (University College London)
Plasticité des représentations corticales motrices après accident vasculaire cérébral
Ahdab, R. (2010) · theses.fr (ABES) · doi:10.70675/e6191692z14b2z401dz9787z00908975d089
Natural Frequencies of Levodopa‐Induced Dyskinesia in Parkinson's Disease
Isaias, I. U., Avantaggiato, F., Pezzoli, G., & Canessa, A. (2026) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.70475
Brain correlates of uncertain decisions: Types and degrees of uncertainty
Volz, K. G. (2004) · Max Planck Institute for Plasma Physics
Metadata
- Authors
- Shima, K., & Tanji, J.
- Affiliations
- Tohoku University (JP)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1998-12-01
- Volume
- 80
- Issue
- 6
- Pages
- 3247-3260
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1773066619
- Cited by
- 272
- References
- 37
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 15 · 2023: 10 · 2022: 7 · 2021: 11 · 2020: 6 · 2019: 12 · 2018: 9 · 2017: 10 · 2016: 11 · 2015: 7 · 2014: 8 · 2013: 17 · 2012: 14
- FWCI
- 3.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- supplementary motor area, pre-supplementary motor area, motor sequence learning, muscimol inactivation
- MeSH terms
- Animals, Forearm, Macaca, Microinjections, Motor Cortex, Movement, Muscimol, Neurons, Psychomotor Performance, Reaction Time, GABA Antagonists
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review