Neural representation of time in cortico-basal ganglia circuits

Jin, Dezhe Z.; Fujii, Naotaka; Graybiel, Ann M.

doi:10.1073/pnas.0909881106

Cited by 246Neural dynamics and brain functionMemory and Neural MechanismsNeural and Behavioral Psychology Studies

Neural representation of time in cortico-basal ganglia circuits

Open access

Jin, Dezhe Z., Fujii, Naotaka, Graybiel, Ann M.·2009·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0909881106PMC PMC2776432

Open this paper in CoChat — free account

Abstract

Encoding time is universally required for learning and structuring motor and cognitive actions, but how the brain keeps track of time is still not understood. We searched for time representations in cortico-basal ganglia circuits by recording from thousands of neurons in the prefrontal cortex and striatum of macaque monkeys performing a routine visuomotor task. We found that a subset of neurons exhibited time-stamp encoding strikingly similar to that required by models of reinforcement-based learning: They responded with spike activity peaks that were distributed at different time delays after single task events. Moreover, the temporal evolution of the population activity allowed robust decoding of task time by perceptron models. We suggest that time information can emerge as a byproduct of event coding in cortico-basal ganglia circuits and can serve as a critical infrastructure for behavioral learning and performance.

Integrity signals

Registry

Crossref · 10.1073/pnas.0909881106

Cites

48 of 48 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

The activity of neurons varied substantially in different trial epochs (99% of neurons, 675/681, ANOVA p<0.05).
“Consistent with previous studies23-25, we found that the activity of neurons varied substantially in different trial epochs (99% of neurons, 675/681, ANOVA p<0.05).”
From A reservoir of time constants for memory traces in cortical neurons (2011) · cites this paper as [25]

Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. G. (1998) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.1998.712192 · Cited by 27,225 · see citing works
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. (2005) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.2004.842673 · Cited by 25,263 · see citing works
The perceptron: A probabilistic model for information storage and organization in the brain.
Rosenblatt, F. (1958) · Psychological Review · doi:10.1037/h0042519 · Cited by 12,280 · see citing works
Self-organized formation of topologically correct feature maps
Kohonen, T. (1982) · Biological Cybernetics · doi:10.1007/bf00337288 · Cited by 9,529 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Self-organized formation of topographically correct feature maps
Kohonen, T. (1982) · Biological Cybernetics · Cited by 2,995 · see citing works
The role of the basal ganglia in habit formation
Yin, H. H., & Knowlton, B. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1919 · Cited by 2,402 · see citing works
Estimation of Dependences Based on Empirical Data
Vapnik, V. N. (2006) · Information science and statistics · doi:10.1007/0-387-34239-7 · Cited by 2,252 · see citing works
What makes us tick? Functional and neural mechanisms of interval timing
Buhusi, C. V., & Meck, W. H. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1764 · Cited by 2,074 · see citing works
A framework for mesencephalic dopamine systems based on predictive Hebbian learning
Montague, P., Dayan, P., & Sejnowski, T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01936.1996 · Cited by 2,066 · see citing works
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
Self-citation
Signal timing across the macaque visual system
Schmolesky, M. T., Wang, Y., Hanes, D. P., Thompson, K. G., Leutgeb, S., Schall, J. D., & Leventhal, A. G. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.6.3272 · Cited by 1,032 · see citing works
The neural basis of temporal processing
Mauk, M. D., & Buonomano, D. V. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144247 · Cited by 976 · see citing works
Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes
Matell, M. S., & Meck, W. H. (2004) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2004.06.012 · Cited by 877 · 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
Estimation of Dependences Based on Empirical Data.
Shoesmith, E., Vapnik, V. N., & Kotz, S. (1984) · Journal of the Royal Statistical Society Series D (The Statistician) · doi:10.2307/2988246 · Cited by 773 · 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
Dissociation of the lateral and medial cerebellum in movement timing and movement execution
Ivry, R. B., Keele, S. W., & Diener, H. C. (1988) · Experimental Brain Research · doi:10.1007/bf00279670 · Cited by 678 · see citing works
Functional Anatomy of the Attentional Modulation of Time Estimation
Coull, J. T., Vidal, F., Nazarian, B., & Macar, F. (2004) · Science · doi:10.1126/science.1091573 · Cited by 642 · see citing works
The representation of temporal information in perception and motor control
Ivry, R. B. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80037-7 · Cited by 639 · see citing works
Representation of Time by Neurons in the Posterior Parietal Cortex of the Macaque
Leon, M. I., & Shadlen, M. N. (2003) · Neuron · doi:10.1016/s0896-6273(03)00185-5 · Cited by 601 · see citing works
Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories
Barnes, T. D., Kubota, Y., Hu, D., Jin, D. Z., & Graybiel, A. M. (2005) · Nature · doi:10.1038/nature04053 · Cited by 595 · see citing works
Self-citation
Timing in the Absence of Clocks: Encoding Time in Neural Network States
Karmarkar, U. R., & Buonomano, D. V. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.006 · Cited by 580 · see citing works
Cortical Networks Underlying Mechanisms of Time Perception
Harrington, D. L., Haaland, K. Y., & Knight, R. T. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-03-01085.1998 · Cited by 561 · see citing works
Temporal Information Transformed into a Spatial Code by a Neural Network with Realistic Properties
Buonomano, D. V., & Merzenich, M. M. (1995) · Science · doi:10.1126/science.7863330 · Cited by 455 · see citing works
The timing of information transfer in the visual system
Nowak, L. G., & Bullier, J. (1997) · Cerebral cortex · doi:10.1007/978-1-4757-9625-4_5 · Cited by 444 · see citing works
Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms
Funahashi, S., Bruce, C. J., & Goldman‐Rakic, P. S. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.4.814 · Cited by 443 · see citing works
Cortico-striatal representation of time in animals and humans
Meck, W. H., Penney, T. B., & Pouthas, V. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.08.002 · Cited by 368 · see citing works
Neural dynamics of adaptive timing and temporal discrimination during associative learning
Grossberg, S., & Schmajuk, N. A. (1989) · Neural Networks · doi:10.1016/0893-6080(89)90026-9 · Cited by 367 · see citing works
Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons.
Matell, M. S., Meck, W. H., & Nicolelis, M. A. L. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.760 · Cited by 352 · see citing works
Timing and Neural Encoding of Somatosensory Parametric Working Memory in Macaque Prefrontal Cortex
Brody, C. D. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg100 · Cited by 350 · see citing works
Decoding Temporal Information: A Model Based on Short-Term Synaptic Plasticity
Buonomano, D. V. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-03-01129.2000 · Cited by 344 · see citing works
Timing Mechanisms in the Cerebellum: Testing Predictions of a Large-Scale Computer Simulation
Medina, J. F., Garcia, K. S., Nores, W. L., Taylor, N. M., & Mauk, M. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-14-05516.2000 · Cited by 343 · see citing works
The temporal precision of reward prediction in dopamine neurons
Fiorillo, C. D., Newsome, W. T., & Schultz, W. (2008) · Nature Neuroscience · doi:10.1038/nn.2159 · Cited by 310 · see citing works
The Storage of Time Intervals Using Oscillating Neurons
Miall, C. (1989) · Neural Computation · doi:10.1162/neco.1989.1.3.359 · Cited by 254 · see citing works
Neuronal Tuning: To Sharpen or Broaden?
Zhang, K., & B, T. J. S. A. (1999) · Neural Computation · doi:10.1162/089976699300016809 · Cited by 253 · see citing works
Neural network involved in time perception: An fMRI study comparing long and short interval estimation
Pouthas, V., George, N., Poline, J., Pfeuty, M., VandeMoorteele, P.-F., Hugueville, L., Ferrandez, A., Lehéricy, S., Bihan, D. L., & Renault, B. (2005) · Human Brain Mapping · doi:10.1002/hbm.20126 · Cited by 223 · see citing works
Latency and Selectivity of Single Neurons Indicate Hierarchical Processing in the Human Medial Temporal Lobe
Mormann, F., Kornblith, S., Quiroga, R. Q., Kraskov, A., Cerf, M., Fried, I., & Christof Koch, A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1640-08.2008 · Cited by 212 · see citing works
Processing of temporal information and the basal ganglia: new evidence from fMRI
Nenadić, I., Christian Gaser, B., Volz, H., Rammsayer, T. H., Häger, F., & Sauer, H. (2003) · Experimental Brain Research · doi:10.1007/s00221-002-1188-4 · Cited by 199 · see citing works
Representation of Action Sequence Boundaries by Macaque Prefrontal Cortical Neurons
Fujii, N., & Graybiel, A. M. (2003) · Science · doi:10.1126/science.1086872 · Cited by 193 · see citing works
Self-citation
Brain Activation Induced by Estimation of Duration: A PET Study
Maquet, P., Lejeune, H., Pouthas, V., Bonnet, M., Casini, L. A., Macar, F., Timsit-Berthier, M., Vidal, F., Ferrara, A., Degueldre, C., et al. (1996) · NeuroImage · doi:10.1006/nimg.1996.0014 · Cited by 188 · see citing works
The Coordinated Mapping of Visual Space and Response Features in Visual Cortex
Yu, H., Farley, B. J., Jin, D. Z., & Sur, M. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.011 · Cited by 125 · see citing works
Self-citation
Cortical Networks Recruited for Time Perception: A Monkey Positron Emission Tomography (PET) Study
Onoe, H., Komori, M., Onoe, K., Takechi, H., Tsukada, H., & Watanabe, Y. (2001) · NeuroImage · doi:10.1006/nimg.2000.0670 · Cited by 124 · see citing works
The neuroanatomical substrate of sound duration discrimination
Belin, P., McAdams, S. E., Thivard, L., Smith, B. K., Savel, S., Zilbovicius, M., Samson, S., & Samson, Y. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00062-3 · Cited by 119 · see citing works
The Representation of Time for Motor Learning
Medina, J. F., Carey, M. R., & Lisberger, S. G. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.017 · Cited by 89 · see citing works
Development of Neural Circuitry for Precise Temporal Sequences through Spontaneous Activity, Axon Remodeling, and Synaptic Plasticity
Jun, J. K., & Jin, D. Z. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000723 · Cited by 87 · see citing works
Self-citation
Time-varying covariance of neural activities recorded in striatum and frontal cortex as monkeys perform sequential-saccade tasks
Fujii, N., & Graybiel, A. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503541102 · Cited by 73 · see citing works
Self-citation
Vergence-mediated changes in the axis of eye rotation during the human vestibulo-ocular reflex can occur independent of eye position
Migliaccio, A. A., Cremer, P. D., Aw, S. T., Halmagyi, G. M., Curthoys, I. S., Minor, L. B., & Todd, M. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1447-z · Cited by 47 · see citing works

Flagged first, then by citations

1 of the 49 references couldn’t be matched to a known paper.

Sorted by citations

Neuroanatomical and Neurochemical Substrates of Timing
Coull, J. T., Cheng, R., & Meck, W. H. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.113 · Cited by 810 · see citing works
Timing and Time Perception
Kononowicz, T. W., van Rijn, H., & Meck, W. H. (2018) · Wiley eBooks · doi:10.1002/9781119170174.epcn114 · Cited by 763 · see citing works
Neural Basis of the Perception and Estimation of Time
Merchant, H., Harrington, D. L., & Meck, W. H. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170349 · Cited by 710 · see citing works
The Neural Representation of Sequences: From Transition Probabilities to Algebraic Patterns and Linguistic Trees
Dehaene, S., Meyniel, F., Wacongne, C., Wang, L., & Pallier, C. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.019 · Cited by 478 · see citing works
Integrating time from experience in the lateral entorhinal cortex
Tsao, A., Sugar, J., Lu, L., Wang, C., Knierim, J. J., Moser, M.-B., & Moser, E. I. (2018) · Nature · doi:10.1038/s41586-018-0459-6 · Cited by 490 · see citing works
Flexible timing by temporal scaling of cortical responses
Wang, J., Narain, D., Hosseini, E. A., & Jazayeri, M. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0028-6 · Cited by 425 · see citing works
The Neural Basis of Timing: Distributed Mechanisms for Diverse Functions
Paton, J. J., & Buonomano, D. V. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.045 · Cited by 449 · see citing works
The inner sense of time: how the brain creates a representation of duration
Wittmann, M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3452 · Cited by 397 · see citing works
A Scalable Population Code for Time in the Striatum
Mello, G. B. M. E., Soares, S., & Paton, J. J. (2015) · Current Biology · doi:10.1016/j.cub.2015.02.036 · Cited by 393 · see citing works
Properties of the Internal Clock: First- and Second-Order Principles of Subjective Time
Allman, M. J., Teki, S., Griffiths, T. D., & Meck, W. H. (2013) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115117 · Cited by 388 · see citing works
Recurrent network models of sequence generation and memory
Rajan, K., Harvey, C. D., & Tank, D. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.009 · Cited by 351 · see citing works
A reservoir of time constants for memory traces in cortical neurons
Bernacchia, A., Seo, H., Lee, D., & Wang, X.-J. (2011) · Nature Neuroscience · doi:10.1038/nn.2752 · Cited by 292 · see citing works
Interval Tuning in the Primate Medial Premotor Cortex as a General Timing Mechanism
Merchant, H., Pérez, O., Zarco, W., & Gámez, J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5513-12.2013 · Cited by 229 · see citing works
A Unified Model of Time Perception Accounts for Duration-Based and Beat-Based Timing Mechanisms
Teki, S., Grube, M., & Griffiths, T. D. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00090 · Cited by 229 · see citing works
Measuring time with different neural chronometers during a synchronization-continuation task
Merchant, H., Zarco, W., Pérez, O., Prado, L., & Bartolo, R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112933108 · Cited by 208 · see citing works
Striatal dynamics explain duration judgments
Gouvêa, T. S., Monteiro, T., Motiwala, A., Soares, S., Machens, C. K., & Paton, J. J. (2015) · eLife · doi:10.7554/elife.11386 · Cited by 203 · see citing works
Information Processing in the Primate Basal Ganglia during Sensory-Guided and Internally Driven Rhythmic Tapping
Bartolo, R., Prado, L., & Merchant, H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2679-13.2014 · Cited by 179 · see citing works
Population clocks: motor timing with neural dynamics
Buonomano, D. V., & Laje, R. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.09.002 · Cited by 183 · see citing works
Action Selection and Action Value in Frontal-Striatal Circuits
Seo, M., Lee, E., & Averbeck, B. B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.037 · Cited by 161 · see citing works
Differential Encoding of Time by Prefrontal and Striatal Network Dynamics
Bakhurin, K. I., Goudar, V., Shobe, J. L., Claar, L. D., Buonomano, D. V., & Masmanidis, S. C. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1789-16.2016 · Cited by 146 · see citing works
Oscillatory multiplexing of neural population codes for interval timing and working memory
Gu, B.-M., van Rijn, H., & Meck, W. H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.008 · Cited by 155 · see citing works
A dual-pathway neural architecture for specific temporal prediction
Schwartze, M., & Kotz, S. A. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.08.005 · Cited by 149 · see citing works
Time Slices: What Is the Duration of a Percept?
Herzog, M. H., Kammer, T., & Scharnowski, F. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002433 · Cited by 144 · see citing works
Evidence for a subcircuit in medial entorhinal cortex representing elapsed time during immobility
Heys, J. G., & Dombeck, D. A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0252-8 · Cited by 139 · see citing works
Decoupling Interval Timing and Climbing Neural Activity: A Dissociation between CNV and N1P2 Amplitudes
Kononowicz, T. W., & van Rijn, H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2523-13.2014 · Cited by 129 · see citing works
Chronotopic maps in human supplementary motor area
Protopapa, F., Hayashi, M. J., Kulashekhar, S., van der Zwaag, W., Battistella, G., Murray, M. M., Ryota Kanai, C., & Bueti, D. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000026 · Cited by 127 · see citing works
Dopamine Precursor Depletion Impairs Timing in Healthy Volunteers by Attenuating Activity in Putamen and Supplementary Motor Area
Coull, J. T., Hwang, H. J., Leyton, M., & Dagher, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1258-12.2012 · Cited by 119 · see citing works
STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning
Kappel, D., Nessler, B., & Maass, W. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003511 · Cited by 112 · see citing works
A temporal record of the past with a spectrum of time constants in the monkey entorhinal cortex
Bright, I. M., Meister, M. L. R., Cruzado, N. A., Tiganj, Z., Buffalo, E. A., & Howard, M. W. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1917197117 · Cited by 99 · see citing works
The neural bases for timing of durations
Tsao, A., Yousefzadeh, S. A., Meck, W. H., Moser, M., & Moser, E. I. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00623-3 · Cited by 109 · see citing works
Evaluating the TD model of classical conditioning
Ludvig, E. A., Sutton, R. S., & Kehoe, E. J. (2012) · Learning & Behavior · doi:10.3758/s13420-012-0082-6 · Cited by 106 · see citing works
Time Adaptation Shows Duration Selectivity in the Human Parietal Cortex
Hayashi, M. J., Ditye, T., Harada, T., Hashiguchi, M., Sadato, N., Carlson, S., Walsh, V., & Ryota Kanai, C. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002262 · Cited by 100 · see citing works
Learning multiple variable-speed sequences in striatum via cortical tutoring
Murray, J. M., & Escola, G. S. (2017) · eLife · doi:10.7554/elife.26084 · Cited by 97 · see citing works
Zebrafish forebrain and temporal conditioning
Cheng, R., Jesuthasan, S. J., & Penney, T. B. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0462 · Cited by 97 · see citing works
Timing as an intrinsic property of neural networks: evidence from in vivo and in vitro experiments
Goel, A., & Buonomano, D. V. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0460 · Cited by 95 · see citing works
The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
Gámez, J., Mendoza, G., Prado, L., Betancourt, A., & Merchant, H. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000054 · Cited by 88 · see citing works
Investigating habits: strategies, technologies and models
Smith, K. S., & Graybiel, A. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00039 · Cited by 92 · see citing works
Self-citation
Population-wide distributions of neural activity during perceptual decision-making
Wohrer, A., Humphries, M. D., & Machens, C. K. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.09.004 · Cited by 89 · see citing works
Compressed Timeline of Recent Experience in Monkey Lateral Prefrontal Cortex
Tiganj, Z., Cromer, J. A., Roy, J. E., Miller, E. K., & Howard, M. W. (2018) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01273 · Cited by 85 · see citing works
Time representation in reinforcement learning models of the basal ganglia
Gershman, S. J., Moustafa, A. A., & Ludvig, E. A. (2014) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2013.00194 · Cited by 81 · see citing works
Sequential and efficient neural-population coding of complex task information
Koay, S. A., Charles, A. S., Thiberge, S. Y., Brody, C. D., & Tank, D. W. (2021) · Neuron · doi:10.1016/j.neuron.2021.10.020 · Cited by 75 · see citing works
A Compact Statistical Model of the Song Syntax in Bengalese Finch
Jin, D. Z., & Kozhevnikov, A. A. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1001108 · Cited by 75 · see citing works
Self-citation
Understanding the computation of time using neural network models
Bi, Z., & Zhou, C. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921609117 · Cited by 63 · see citing works
A neural circuit model for human sensorimotor timing
Egger, S. W., Le, N. M., & Jazayeri, M. (2020) · Nature Communications · doi:10.1038/s41467-020-16999-8 · Cited by 74 · see citing works
Habit formation coincides with shifts in reinforcement representations in the sensorimotor striatum
Smith, K. S., & Graybiel, A. M. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00925.2015 · Cited by 64 · see citing works
Self-citation
Acquisition of “Start” and “Stop” response thresholds in peak-interval timing is differentially sensitive to protein synthesis inhibition in the dorsal and ventral striatum
MacDonald, C. J., Cheng, R., & Meck, W. H. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00010 · Cited by 67 · see citing works
Explicit Understanding of Duration Develops Implicitly through Action
Coull, J. T., & Droit‐Volet, S. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.07.011 · Cited by 68 · see citing works
Learning spatiotemporal signals using a recurrent spiking network that discretizes time
Maes, A., Barahona, M., & Claudia Clopath, A. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007606 · Cited by 63 · see citing works
Neurocomputational models of interval and pattern timing
Hardy, N. F., & Buonomano, D. V. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.01.012 · Cited by 58 · see citing works
A basal ganglia-like cortical–amygdalar–hypothalamic network mediates feeding behavior
Barbier, M., Chometton, S., Pautrat, A., Miguet‐Alfonsi, C., Datiche, F., Gascuel, J., FELLMANN, D., Peterschmitt, Y., Coizet, V., & Risold, P. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004914117 · Cited by 60 · see citing works
Ensembles of Spiking Neurons with Noise Support Optimal Probabilistic Inference in a Dynamically Changing Environment
Legenstein, R. A., & Maass, W. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003859 · Cited by 54 · see citing works
Time Crawls When You’re Not Having Fun
O'Brien, E. H., Anastasio, P. A., & Bushman, B. (2011) · Personality and Social Psychology Bulletin · doi:10.1177/0146167211408922 · Cited by 60 · see citing works
Singing-Related Neural Activity Distinguishes Four Classes of Putative Striatal Neurons in the Songbird Basal Ganglia
Goldberg, J. H., & Fee, M. S. (2010) · Journal of Neurophysiology · doi:10.1152/jn.01038.2009 · Cited by 58 · see citing works
Predicting the Future with Multi-scale Successor RepresentationsPreprint
Momennejad, I., & Howard, M. W. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/449470 · Cited by 59 · see citing works
Oscillatory recurrent gated neural integrator circuits (ORGaNICs), a unifying theoretical framework for neural dynamics
Heeger, D. J., & Mackey, W. E. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911633116 · Cited by 54 · see citing works
Memory as Perception of the Past: Compressed Time inMind and Brain
Howard, M. W. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.11.004 · Cited by 58 · see citing works
Distributed Representations of Rule Identity and Rule Order in Human Frontal Cortex and Striatum
Reverberi, C., Görgen, K., & Haynes, J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2344-12.2012 · Cited by 53 · see citing works
Altered functional connectivity in persistent developmental stuttering
Yang, Y., Jia, F., Siok, W. T., & Tan, L. H. (2016) · Scientific Reports · doi:10.1038/srep19128 · Cited by 52 · see citing works
A neural microcircuit model for a scalable scale‐invariant representation of time
Liu, Y., Tiganj, Z., Hasselmo, M. E., & Howard, M. W. (2018) · Hippocampus · doi:10.1002/hipo.22994 · Cited by 52 · see citing works
Exploring the 4th Dimension: Hippocampus, Time, and Memory Revisited
Yin, B., & Troger, A. B. (2011) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00036 · Cited by 51 · see citing works
Ramping single unit activity in the medial prefrontal cortex and ventral striatum reflects the onset of waiting but not imminent impulsive actions
Donnelly, N. A., Paulsen, O., Robbins, T. W., & Dalley, J. W. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12895 · Cited by 49 · see citing works
Modulation of Human Time Processing by Subthalamic Deep Brain Stimulation
Wojtecki, L., Elben, S., Timmermann, L., Reck, C., Maarouf, M., Jörgens, S., Ploner, M., Südmeyer, M., Groiss, S. J., Sturm, V., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024589 · Cited by 51 · see citing works
A model of temporal scaling correctly predicts that motor timing improves with speed
Hardy, N. F., Goudar, V., Romero-Sosa, J. L., & Buonomano, D. V. (2018) · Nature Communications · doi:10.1038/s41467-018-07161-6 · Cited by 54 · see citing works
Conjunctive representation of what and when in monkey hippocampus and lateral prefrontal cortex during an associative memory task
Cruzado, N. A., Tiganj, Z., Brincat, S. L., Miller, E. K., & Howard, M. W. (2020) · Hippocampus · doi:10.1002/hipo.23282 · Cited by 43 · see citing works
Using temperature to analyze the neural basis of a time-based decision
Monteiro, T., Rodrigues, F. S., Pexirra, M., Cruz, B. F., Gonçalves, A. I., Rueda‐Orozco, P. E., & Paton, J. J. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01378-5 · Cited by 48 · see citing works
Temporal Processing in Audition: Insights from Music
Rajendran, V. G., Teki, S., & Schnupp, J. W. H. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.10.041 · Cited by 44 · see citing works
Navigating Through Time: A Spatial Navigation Perspective on How the Brain May Encode Time
Issa, J. B., Tocker, G., Hasselmo, M. E., Heys, J. G., & Dombeck, D. A. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-101419-011117 · Cited by 46 · see citing works
Neurocomputational Models of Time Perception
Haß, J., & Durstewitz, D. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1782-2_4 · Cited by 47 · see citing works
Temporal Perceptual Learning
Bueti, D., & Buonomano, D. V. (2014) · Timing & Time Perception · doi:10.1163/22134468-00002023 · Cited by 46 · see citing works
Optimal Balance of the Striatal Medium Spiny Neuron Network
Ponzi, A. P. D., & Wickens, J. R. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002954 · Cited by 44 · see citing works
Encoding Time in Feedforward Trajectories of a Recurrent Neural Network Model
Hardy, N. F., & Buonomano, D. V. (2017) · Neural Computation · doi:10.1162/neco_a_01041 · Cited by 43 · see citing works
Neural processes underlying statistical learning for speech segmentation in dogs
Boros, M., Magyari, L., Török, D., Bozsik, A., Deme, A., & Andics, A. (2021) · Current Biology · doi:10.1016/j.cub.2021.10.017 · Cited by 33 · see citing works
A Neural Model for Temporal Order Judgments and Their Active Recalibration: A Common Mechanism for Space and Time?
Cai, M. B., Stetson, C., & Eagleman, D. M. (2012) · Frontiers in Psychology · doi:10.3389/fpsyg.2012.00470 · Cited by 41 · see citing works
Choice-selective sequences dominate in cortical relative to thalamic inputs to NAc to support reinforcement learning
Parker, N. F., Baidya, A., Cox, J., Haetzel, L. M., Zhukovskaya, A., Murugan, M., Engelhard, B., Goldman, M. S., & Witten, I. B. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110756 · Cited by 38 · see citing works
Significance of Input Correlations in Striatal Function
Yim, M. Y., Aertsen, A., & Kumar, A. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002254 · Cited by 39 · see citing works
Internally generated time in the rodent hippocampus is logarithmically compressed
Cao, R., Bladon, J. H., Charczynski, S. J., Hasselmo, M. E., & Howard, M. W. (2022) · eLife · doi:10.7554/elife.75353 · Cited by 37 · see citing works
A quantitative analysis of information about past and present stimuli encoded by spikes of A1 neurons
Klampfl, S., David, S. V., Yin, P., Shamma, S., & Maass, W. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00935.2011 · Cited by 38 · see citing works
Time coding in rat dorsolateral striatum
Toso, A., Reinartz, S., Pulecchi, F., & Diamond, M. E. (2021) · Neuron · doi:10.1016/j.neuron.2021.08.020 · Cited by 38 · see citing works
Neurophysiology of Timing in the Hundreds of Milliseconds: Multiple Layers of Neuronal Clocks in the Medial Premotor Areas
Merchant, H., Bartolo, R., Pérez, O., Méndez, J. C., Mendoza, G., Gámez, J., Yc, K., & Prado, L. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1782-2_8 · Cited by 38 · see citing works
Sensory-spatial transformations in the left posterior parietal cortex may contribute to reach timing.
Torres, E., Raymer, A. L., Rothi, L. G. G., Heilman, K., & Poizner, H. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00089.2010 · Cited by 32 · see citing works
Learning of Temporal Motor Patterns: An Analysis of Continuous Versus Reset Timing
Laje, R., Cheng, K. Y., & Buonomano, D. V. (2011) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2011.00061 · Cited by 35 · see citing works
A Neural Correlate of the Processing of Multi-Second Time Intervals in Primate Prefrontal Cortex
Yumoto, N., Lu, X., Henry, T. R., Miyachi, S., Nambu, A., Fukai, T., & Takada, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019168 · Cited by 35 · see citing works
Effects of methylphenidate on basic and higher-order oculomotor functions
Allman, A.-A., Ettinger, U., Joober, R., & O’Driscoll, G. A. (2012) · Journal of Psychopharmacology · doi:10.1177/0269881112446531 · Cited by 35 · see citing works
The hippocampus contributes to temporal duration memory in the context of event sequences: A cross-species perspective
Lee, A. C. H., Thavabalasingam, S., Alushaj, D., Çavdaroğlu, B., & Ito, R. (2019) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2019.107300 · Cited by 35 · see citing works
Time as the fourth dimension in the hippocampus
Banquet, J. P., Gaussier, P., Cuperlier, N., Hok, V., Save, É., Poucet, B., Quoy, M., & Wiener, S. I. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101920 · Cited by 33 · see citing works
The functional neuroanatomy of serial order in language
Boeckx, C. A., Martinez‐Alvarez, A., & Leivada, E. (2014) · Journal of Neurolinguistics · doi:10.1016/j.jneuroling.2014.07.001 · Cited by 32 · see citing works
From space to time: Spatial inhomogeneities lead to the emergence of spatiotemporal sequences in spiking neuronal networks
Spreizer, S., Aertsen, A., & Kumar, A. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007432 · Cited by 32 · see citing works
Acquisition of response thresholds for timed performance is regulated by a calcium‐responsive transcription factor, CaRF
Agostino, P. V., Cheng, R. ‐., Williams, C. L., West, A. E., & Meck, W. H. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12059 · Cited by 31 · see citing works
Ongoing behavior predicts perceptual report of interval duration
Gouvêa, T. S., Monteiro, T., Soares, S., Atallah, B. V., & Paton, J. J. (2014) · Frontiers in Neurorobotics · doi:10.3389/fnbot.2014.00010 · Cited by 31 · see citing works
Input Dependent Cell Assembly Dynamics in a Model of the Striatal Medium Spiny Neuron Network
Ponzi, A. P. D., & Wickens, J. R. (2012) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00006 · Cited by 32 · see citing works
Neural encoding of time in the animal brain
Tallot, L., & Doyère, V. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.033 · Cited by 27 · see citing works
Transitioning between preparatory and precisely sequenced neuronal activity in production of a skilled behavior
Daliparthi, V., Tachibana, R. O., Cooper, B. G., Hahnloser, R. H. R., Kojima, S., Sober, S. J., & Roberts, T. F. (2019) · eLife · doi:10.7554/elife.43732 · Cited by 29 · see citing works
Encoding time in neural dynamic regimes with distinct computational tradeoffs
Zhou, S., Masmanidis, S. C., & Buonomano, D. V. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009271 · Cited by 23 · see citing works
Impact of Auditory Context on Executed Motor Actions
Yoles-Frenkel, M., Avron, M., & Prut, Y. (2016) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2016.00001 · Cited by 27 · see citing works
Predictive Motor Timing and the Cerebellar Vermis in Schizophrenia: An fMRI Study
Lošák, J., Hüttlová, J., Lipová, P., Mareček, R., Bareš, M., Filip, P., Žůbor, J., Ustohal, L., Vaníček, J., & Kašpárek, T. (2016) · Schizophrenia Bulletin · doi:10.1093/schbul/sbw065 · Cited by 24 · see citing works
Neural Dynamics Based Timing in the Subsecond to Seconds Range
Buonomano, D. V. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-1782-2_6 · Cited by 23 · see citing works
Covert spatial selection in primate basal ganglia
Arcizet, F., & Krauzlis, R. J. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2005930 · Cited by 23 · see citing works
The ecological significance of time sense in animals
Ng, L., García, J. E., Dyer, A. G., & Stuart-Fox, D. M. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12665 · Cited by 22 · see citing works
Neuronal representation of duration discrimination in the monkey striatum
Chiba, A., Oshio, K., & Inase, M. (2015) · Physiological Reports · doi:10.14814/phy2.12283 · Cited by 22 · see citing works
Altered Time Awareness in Dementia
Requena‐Komuro, M., Marshall, C. R., Bond, R. L., Russell, L. L., Greaves, C. V., Moore, K. M., Agustus, J. L., Benhamou, E., Sivasathiaseelan, H., Hardy, C. J. D., et al. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00291 · Cited by 21 · see citing works

Differential Encoding of Time by Prefrontal and Striatal Network Dynamics
Bakhurin, K. I., Goudar, V., Shobe, J. L., Claar, L. D., Buonomano, D. V., & Masmanidis, S. C. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1789-16.2017 · Cited by 6 · see citing works
62 Neural Correlates of Cognitive Function in the Basal Ganglia
Hunter, C. M., Khandelwal, V., & Narayanan, N. S. (2023) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617723006124
Time-varying covariance of neural activities recorded in striatum and frontal cortex as monkeys perform sequential-saccade tasks
Fujii, N., & Graybiel, A. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503541102 · Cited by 73 · see citing works
Self-citation
Decoding of temporal intervals from cortical ensemble activity.
Lebedev, M., O'Doherty, J. E., & Nicolelis, M. (2008) · Journal of Neurophysiology · doi:10.1152/jn.00734.2007 · Cited by 163 · see citing works
Ensemble neural activity of the frontal cortical basal ganglia system predicts reaction time task performance in rats
Li, X., Luo, F., Shi, L., Woodward, D. J., & Chang, J. (2011) · Neuroscience Research · doi:10.1016/j.neures.2011.06.010 · Cited by 4 · see citing works

Authors: Jin, D. Z., Fujii, N., & Graybiel, A. M.
Affiliations: Pennsylvania State University (US)
RIKEN Center for Brain Science (JP)
McGovern Institute for Brain Research (US)
ORCID: Jin, Dezhe Z.
Fujii, Naotaka
Graybiel, Ann M.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2009-11-10
Volume: 106
Issue: 45
Pages: 19156-19161
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0909881106
PMC: PMC2776432
OpenAlex: W2156530149
Cited by: 246
References: 49
Citations by year: 2026: 13 · 2025: 11 · 2024: 20 · 2023: 8 · 2022: 16 · 2021: 11 · 2020: 16 · 2019: 14 · 2018: 20 · 2017: 12 · 2016: 17 · 2015: 14 · 2014: 20 · 2013: 11 · 2012: 18
FWCI: 6.77
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
Funders: National Eye Institute (EY12848, R01EY012848)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: cortico-basal ganglia circuits, prefrontal cortex, striatum, reinforcement learning, macaque, visuomotor task, event coding
MeSH terms: Algorithms, Animals, Basal Ganglia, Brain Mapping, Electrophysiology, Macaca mulatta, Models, Psychological, Neural Pathways, Psychomotor Performance, Saccades, Time, Prefrontal Cortex

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

Neural representation of time in cortico-basal ganglia circuits

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks