Neural systems supporting timing and chronometric counting: an FMRI study
Open accessAbstract
At least two strategies are available to humans for estimating multisecond intervals. One depends on an interval timing system that is common to many species. The other is the language-based strategy of chronometric counting. These two strategies are easily distinguished by the psychophysical properties of their behavioral correlates: counting supports substantially more precise estimates than are possible using the more general interval timing system. The present study investigates the neural systems that underlie the execution of these different strategies. Eighteen adults reproduced a 16-s interval either by internally timing or covertly counting the duration. Comparison of counting and timing to a resting baseline suggested that these strategies engage some nonoverlapping neural systems. Counting, but not timing, strongly activated Broca's area, primary motor cortex in the mouth region, and right cerebellum, all of which are associated with internal speech. Counting also activated parts of the medial premotor circuit, including the putamen, supplementary motor area (SMA) proper, and cingulate motor area (CMA), that have been associated with reproducing isochronous and syncopated rhythms of elements lasting hundreds of milliseconds. During timing, only a portion of this circuit, the SMA proper and CMA, was engaged. Both timing and counting interfered with semantic processing during the resting state, evidenced by task-related decreases in the left inferior and middle frontal gyri, right superior frontal gyrus, left angular gyrus, and bilateral posterior cingulate cortex. This study suggests that counting activates a corticostriatal network associated with millisecond, rhythmic timing. In contrast, timing long durations without the benefit of linguistic strategies for subdividing counts reduces activity in this circuitry.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Left putamen activation is associated with counting and reading written syllables, consistent with the putamen being involved in timing of speech production.
“This might explain why left putamen activation was associated with counting (Hinton et al., 2004) and reading written syllables (Bohland and Guenther, 2006) and is consistent with prior claims that the putamen is involved in the timing of speech production.”
From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Hinton et al., 2004
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A default mode of brain function
Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.2.676 · Cited by 12,190 · see citing works
Co-Planar Stereotaxic Atlas of the Human Brain
Talairach, J., & Tournoux, P. (1988) · Medical Entomology and Zoology · Cited by 11,798 · see citing works
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913 · see citing works
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.09.030186.002041 · Cited by 8,527 · see citing works
Co-planar stereotaxic atlas of the human brain
Laitinen, L. (1989) · Clinical Neurology and Neurosurgery · doi:10.1016/0303-8467(89)90128-5 · Cited by 7,565 · see citing works
Positron emission tomographic studies of the cortical anatomy of single-word processing
Petersen, S. E., Fox, P. T., Posner, M. I., Mintun, M., & Raichle, M. E. (1988) · Nature · doi:10.1038/331585a0 · Cited by 2,593 · see citing works
The neural correlates of the verbal component of working memory
Paulesu, E., Frith, C. D., & Frackowiak, R. S. J. (1993) · Nature · doi:10.1038/362342a0 · Cited by 2,230 · cited 3× · see citing works
“Converging evidence using different tasks and neuroimaging techniques implicates the left inferior frontal cortex (BA 44), left ventral premotor cortex, and right cerebellum in mediating verbal rehearsal [3,22, 42,55,58].”
BackgroundScalar expectancy theory and Weber's law in animal timing.
Gibbon, J. (1977) · Psychological Review · doi:10.1037/0033-295x.84.3.279 · Cited by 2,224 · see citing works
Common blood flow changes across visual tasks: II. Decreases in cerebral cortex
Shulman, G. L., Fiez, J. A., Corbetta, M., Buckner, R. L., Miezin, F. M., Raichle, M. E., & Petersen, S. E. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.5.648 · Cited by 1,890 · see citing works
Gibbon, J., Church, R. M., & Meck, W. H. (1984) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1984.tb23417.x · Cited by 1,806 · see citing works
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 · see citing works
An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex
Essen, D. C. V., Drury, H. A., Dickson, J., Harwell, J., Hanlon, D., & Anderson, C. H. (2001) · Journal of the American Medical Informatics Association · doi:10.1136/jamia.2001.0080443 · Cited by 1,100 · see citing works
A mode control model of counting and timing processes.
Meck, W. H., & Church, R. M. (1983) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.9.3.320 · Cited by 1,055 · see citing works
Neuropharmacology of timing and time perception
Meck, W. H. (1996) · Cognitive Brain Research · doi:10.1016/0926-6410(96)00009-2 · Cited by 952 · see citing works
Mazoyer, B., Zago, L., Mellet, E., Bricogne, S., Etard, O., Houdé, O., Crivello, F., Joliot, M., Petit, L., & Tzourio-Mazoyer, N. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00437-8 · Cited by 906 · see citing works
The evolution of brain activation during temporal processing
Rao, S. M., Mayer, A. R., & Harrington, D. L. (2001) · Nature Neuroscience · doi:10.1038/85191 · Cited by 827 · see citing works
Self-citationThe Theory of reinforcement schedules
SCHOENFELD, W. N. (1970) · Appleton-Century-Crofts eBooks · Cited by 799 · see citing works
Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space
Schmahmann, J. D., Doyon, J., McDonald, D., Holmes, C. J., Lavoie, K., Hurwitz, A. S., Kabani, N. J., Toga, A. W., Evans, A. C., & Petrides, M. (1999) · NeuroImage · doi:10.1006/nimg.1999.0459 · Cited by 782 · see citing works
Toward a neurobiology of temporal cognition: advances and challenges
Gibbon, J., Malapani, C., Dale, C. L., & Gallistel, C. R. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80005-0 · Cited by 766 · see citing works
When zero is not zero: the problem of ambiguous baseline conditions in fMRI
Stark, C. E. L., & Squire, L. R. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221462998 · Cited by 724 · see citing works
Awh, E., Jonides, J., Smith, E. E., Schumacher, E. H., Koeppe, R. A., & Katz, S. (1996) · Psychological Science · doi:10.1111/j.1467-9280.1996.tb00662.x · Cited by 705 · see citing works
Distributed Neural Systems Underlying the Timing of Movements
Rao, S. M., Harrington, D. L., Haaland, K. Y., Bobholz, J. A., Cox, R. W., & Binder, J. R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-14-05528.1997 · Cited by 665 · see citing works
Self-citationIsolation of an internal clock.
Roberts, S. (1981) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.7.3.242 · Cited by 635 · see citing works
Halsband, U., Ito, N., Tanji, J., & Freund, H. (1993) · Brain · doi:10.1093/brain/116.1.243 · Cited by 549 · see citing works
Desmond, J. E., Gabrieli, J. D. E., Wagner, A. D., Ginier, B. L., & Glover, G. H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09675.1997 · Cited by 530 · see citing works
Functional and Neural Mechanisms of Interval Timing
Meck, W. H. (2003) · CRC Press eBooks · doi:10.1201/9780203009574 · Cited by 522 · see citing works
Brain regions involved in articulation
Wise, R., Greene, J., Büchel, C., & Scott, S. (1999) · The Lancet · doi:10.1016/s0140-6736(98)07491-1 · Cited by 517 · see citing works
Components of verbal working memory: Evidence from neuroimaging
Smith, E. E., Jonides, J. J., Marshuetz, C., & Koeppe, R. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.876 · Cited by 492 · see citing works
Encyclopedia of the human brain
(2003) · Choice Reviews Online · doi:10.5860/choice.40-2552 · Cited by 384 · see citing works
Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction
Penhune, V. B., Zatorre, R. J., & Evans, A. C. (1998) · Journal of Cognitive Neuroscience · doi:10.1162/089892998563149 · Cited by 370 · see citing works
A TWO‐STATE ANALYSIS OF FIXED‐INTERVAL RESPONDING IN THE PIGEON1
Schneider, B. A. (1969) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1969.12-677 · Cited by 351 · see citing works
Neural correlates of lexical access during visual word recognition
Binder, J. R., McKiernan, K. A., Parsons, M. E., Westbury, C. F., Possing, E. T., Kaufman, J. N., & Buchanan, L. (2003) · Journal of Cognitive Neuroscience · doi:10.1162/089892903321593108 · Cited by 344 · see citing works
Self-citationScalar expectancy theory and peak-interval timing in humans.
Rakitin, B. C., Gibbon, J., Penney, T. B., Malapani, C., Hinton, S. C., & Meck, W. H. (1998) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.24.1.15 · Cited by 336 · see citing works
Self-citationAre Subitizing and Counting Implemented as Separate or Functionally Overlapping Processes?
Manuela Piazza, A., Mechelli, A., Butterworth, B. L., & Price, C. J. (2002) · NeuroImage · doi:10.1006/nimg.2001.0980 · Cited by 318 · see citing works
Recoding, storage, rehearsal and grouping in verbal short-term memory: an fMRI study.
Henson, R. N. A., Burgess, N., & Frith, C. (2000) · Neuropsychologia · doi:10.1016/s0028-3932(99)00098-6 · Cited by 310 · see citing works
Functional magnetic resonance imaging of Brocaʼs area during internal speech
Hinke, R. M., Hu, X., Stillman, A. E., Kim, S.-G., Merkle, H., Salmi, R., & Ugurbil, K. (1993) · NeuroReport · doi:10.1097/00001756-199306000-00018 · Cited by 293 · see citing works
The differential effects of haloperidol and methamphetamine on time estimation in the rat
Maricq, A. V., & Church, R. M. (1983) · Psychopharmacology · doi:10.1007/bf00433008 · Cited by 286 · see citing works
Meck, W. H. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90109-7 · Cited by 272 · see citing works
PET Evidence for an Amodal Verbal Working Memory System
Schumacher, E. H., Lauber, E. J., Awh, E., Jonides, J. J., Smith, E. E., & Koeppe, R. A. (1996) · NeuroImage · doi:10.1006/nimg.1996.0009 · Cited by 262 · see citing works
Activation of the supplementary motor area and of attentional networks during temporal processing
Macar, F., Lejeune, H., Bonnet, M., Ferrara, A., Pouthas, V., Vidal, F., & Maquet, P. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0953-0 · Cited by 250 · see citing works
The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes
Macar, F., Vidal, F., & Casini, L. A. (1999) · Experimental Brain Research · doi:10.1007/s002210050683 · Cited by 250 · see citing works
Do humans possess an internal clock with scalar timing properties?
Wearden, J. H. (1991) · Learning and Motivation · doi:10.1016/0023-9690(91)90017-3 · Cited by 220 · see citing works
Temporal integration in duration and number discrimination.
Meck, W. H., Church, R. M., & Gibbon, J. (1985) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.11.4.591 · Cited by 216 · see citing works
New concepts of the supplementary motor area
Tanji, J. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80028-6 · Cited by 216 · see citing works
Grondin, S., Meilleur-Wells, G., & Lachance, R. (1999) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037/0096-1523.25.4.993 · Cited by 206 · see citing works
Lee, T. S., Yang, C. F., Romero, R. D., & Mumford, D. (2002) · Nature Neuroscience · doi:10.1038/nn0602-860 · Cited by 205 · see citing works
Neural representation of interval encoding and decision making
Harrington, D. L., Boyd, L. A., Mayer, A. R., Sheltraw, D., Lee, R. R., Huang, M., & Rao, S. M. (2004) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2004.01.010 · Cited by 196 · see citing works
Self-citationHarrington, D. L., & Haaland, K. Y. (1999) · Reviews in the Neurosciences · doi:10.1515/revneuro.1999.10.2.91 · Cited by 196 · see citing works
Self-citationNeural Evidence Linking Visual Object Enumeration and Attention
Sathian, K., Simon, T. J., Peterson, S., Patel, G. A., Hoffman, J. M., & Grafton, S. T. (1999) · Journal of Cognitive Neuroscience · doi:10.1162/089892999563238 · Cited by 174 · see citing works
Silveri, M. (1998) · Brain · doi:10.1093/brain/121.11.2175 · Cited by 165 · see citing works
Corfield, D. R., Murphy, K., Josephs, O., Fink, G. R., Frackowiak, R. S. J., Guz, A., Adams, L., & Turner, R. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.86.5.1468 · Cited by 146 · see citing works
Reproducibility of primary motor cortex somatotopy under controlled conditions.
Alkadhi, H., Crelier, G. R., Boendermaker, S. H., Golay, X., Hepp‐Reymond, M., & Kollias, S. (2002) · PubMed Central · Cited by 136 · see citing works
Human cerebellum plays an important role in memory-timed finger movement: an fMRI study
Kawashima, R., Okuda, J., Umetsu, A., Sugiura, M., Inoue, K., Suzuki, K., Tabuchi, M., Tsukiura, T., Narayan, S. L., Nagasaka, T., et al. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.2.1079 · Cited by 123 · see citing works
Cortical representation of self-paced finger movement
Larsson, J. T., Gulyás, B. Z., & Roland, P. E. (1996) · Neuroreport · doi:10.1097/00001756-199601310-00021 · Cited by 109 · see citing works
Wearden, J. H., & McShane, B. (2007) · Quarterly Journal of Experimental Psychology · doi:10.1080/14640748808402330 · Cited by 103 · see citing works
The representation of articulation in the primary sensorimotor cortex
Lotze, M., Seggewies, G., Erb, M., Grodd, W., & Birbaumer, N. (2000) · Neuroreport · doi:10.1097/00001756-200009110-00032 · Cited by 100 · see citing works
Hinton, S. C., & Rao, S. M. (2004) · Psychonomic Bulletin & Review · doi:10.3758/bf03206456 · Cited by 90 · see citing works
Self-citationDuration discrimination by rats.
Church, R. M., Getty, D. J., & Lerner, N. (1976) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.2.4.303 · Cited by 87 · see citing works
Vidal, F., Bonnet, M., & Macar, F. (1995) · Experimental Brain Research · doi:10.1007/bf00241129 · Cited by 80 · see citing works
Sustained Attention in a Counting Task: Normal Performance and Functional Neuroanatomy
Ortuño, F., Ojeda, N., Arbizu, J., López-García, P., Martí-Climent, J. M., Peñuelas, I., & Cervera, S. (2002) · NeuroImage · doi:10.1006/nimg.2002.1168 · Cited by 79 · see citing works
A componential analysis of pacemaker-counter timing systems.
Fetterman, J. G., & Killeen, P. R. (1990) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037//0096-1523.16.4.766 · Cited by 64 · see citing works
Duration discrimination by rats.
Church, R. M., Getty, D. J., & Lerner, N. (1976) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.2.4.303 · Cited by 59 · see citing works
Interval schedule performance in the goldfish Carassius auratus
Talton, L. E., Higa, J. J., & Staddon, J. E. R. (1999) · Behavioural Processes · doi:10.1016/s0376-6357(99)00018-2 · Cited by 50 · see citing works
Some factors in estimating short time intervals.
Gilliland, A. R., & Martin, R. (1940) · Journal of Experimental Psychology · doi:10.1037/h0060494 · Cited by 45 · see citing works
Cerebral correlates of working memory for temporal information
Gruber, O., Kleinschmidt, A. K., Binkofski, F., Steinmetz, H., & von Cramon, D. Y. (2000) · Neuroreport · doi:10.1097/00001756-200006050-00019 · Cited by 44 · see citing works
A componential analysis of pacemaker-counter timing systems.
Fetterman, J. G., & Killeen, P. R. (1990) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037/0096-1523.16.4.766 · Cited by 40 · see citing works
Single- and multiple-event paradigms for identification of motor cortex activation.
Marquart, M., Birn, R. M., & Haughton, V. M. (2000) · PubMed · Cited by 10 · see citing works
Neuroimaging Approaches to the Study of Interval Timing
Hinton, S. C. (2003) · Frontiers in neuroscience · doi:10.1201/9780203009574.ch17 · Cited by 10 · see citing works
Self-citationDeterminants of nicotine self-administration
Shoaib, M. C. (1996) · Drug Development Research · doi:10.1002/(sici)1098-2299(199607/08)38:3/4 · Cited by 7 · see citing works
Time Passage, Neural Substrates
Harrington, D. L., & Rao, S. M. (2002) · Elsevier eBooks · doi:10.1016/b0-12-227210-2/00348-4 · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Price, C. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.04.062 · Cited by 2,159 · see citing works
The image of time: A voxel-wise meta-analysis
Wiener, M., Turkeltaub, P., & Coslett, H. B. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.09.064 · Cited by 594 · see citing works
Noreika, V., Falter, C. M., & Rubia, K. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.09.036 · Cited by 339 · see citing works
Neural correlates of lexical access during visual word recognition
Binder, J. R., McKiernan, K. A., Parsons, M. E., Westbury, C. F., Possing, E. T., Kaufman, J. N., & Buchanan, L. (2003) · Journal of Cognitive Neuroscience · doi:10.1162/089892903321593108 · Cited by 344 · see citing works
Self-citationAccumulation of neural activity in the posterior insula encodes the passage of time
Wittmann, M., Simmons, A. N., Aron, J. L., & Paulus, M. P. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.06.023 · Cited by 203 · see citing works
Waltz, J. A., Schweitzer, J. B., Gold, J. M., Kurup, P. K., Ross, T. J., Jo Salmeron, B., Rose, E. J., McClure, S. M., & Stein, E. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.214 · Cited by 186 · see citing works
The role of the human anterior insular cortex in time processing
Kosillo, P., & Smith, A. T. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0267-8 · Cited by 59 · see citing works
Time is body: multimodal evidence of crosstalk between interoception and time estimation
Richter, F., & Ibáñez, A. (2021) · Biological Psychology · doi:10.1016/j.biopsycho.2021.108017 · Cited by 40 · see citing works
- Authors
- Hinton, S. C., Harrington, D. L., Binder, J. R., Durgerian, S., & Rao, S. M.
- Affiliations
- Medical College of Wisconsin (US)
- University of New Mexico (US)
- Corresponding author
- Hinton, Sean C.
- Venue
- Cognitive Brain Research
- Publisher
- Elsevier BV
- Published
- 2004-10
- Volume
- 21
- Issue
- 2
- Pages
- 183-192
- ISSN
- 0926-6410 (ISSN-L)
- OpenAlex
- W2035524700
- Cited by
- 99
- References
- 71
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 7 · 2017: 3 · 2016: 2 · 2015: 4 · 2014: 6 · 2013: 6 · 2012: 11
- FWCI
- 2.35
- Type
- journal article
- Language
- en
- Open access
- green
- escholarship.org
- Locations
- Cognitive Brain Research (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Veterans Affairs
- National Institutes of Health (RR00058)
- National Institute of Mental Health (P01MH51358, P01MH051358)
- National Center for Research Resources (M01-RR00058, M01RR000058)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- interval timing, duration estimation, Broca's area, supplementary motor area, cingulate motor area, corticostriatal network, cerebellum, inner speech, semantic processing, frontal cortex
- MeSH terms
- Adult, Analysis of Variance, Brain, Brain Mapping, Female, Humans, Image Processing, Computer-Assisted, Functional Laterality, Magnetic Resonance Imaging, Male, Mathematics, Middle Aged, Oxygen, Time Factors, Time Perception
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
