Robust timing and motor patterns by taming chaos in recurrent neural networks
Open accessAbstract
The brain's ability to tell time and produce complex spatiotemporal motor patterns is critical for anticipating the next ring of a telephone or playing a musical instrument. One class of models proposes that these abilities emerge from dynamically changing patterns of neural activity generated in recurrent neural networks. However, the relevant dynamic regimes of recurrent networks are highly sensitive to noise; that is, chaotic. We developed a firing rate model that tells time on the order of seconds and generates complex spatiotemporal patterns in the presence of high levels of noise. This is achieved through the tuning of the recurrent connections. The network operates in a dynamic regime that exhibits coexisting chaotic and locally stable trajectories. These stable patterns function as 'dynamic attractors' and provide a feature that is characteristic of biological systems: the ability to 'return' to the pattern being generated in the face of perturbations.
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?
A recurrent neural network is difficult to train and control because it may exhibit chaotic behavior.
“A recurrent neural network is also known to be difficult to train and control because it may exhibit chaotic behavior (Sompolinsky et al., 1988; Sussillo and Abbott, 2009; Laje and Buonomano, 2013; Ben-Shushan and Tsodyks, 2017).”
From The Cerebro-Cerebellum as a Locus of Forward Model: A Review (2020) · cites this paper as Laje and Buonomano, 2013
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
Harnessing Nonlinearity: Predicting Chaotic Systems and Saving Energy in Wireless Communication
Jaeger, H., & Haas, H. (2004) · Science · doi:10.1126/science.1091277 · Cited by 3,811 · see citing works
Stimulus onset quenches neural variability: A widespread cortical phenomenon
Churchland, M. M., Yu, B. M., Cunningham, J. P., Sugrue, L. P., Cohen, M. R., Corrado, G. S., Newsome, W. T., Clark, A. M., Hosseini, P., Scott, B. B., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2501 · Cited by 1,084 · see citing works
Correction: Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits
Song, S., Sjöström, P. J., Reigl, M., Nelson, S., & Chklovskii, D. B. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030350 · Cited by 75 · see citing works
Flagged first, then by citations
Research works printed but not linked: 46
- [1]Mauk MD Buonomano DV The Neural Basis of Temporal Processing Ann. Rev. Neurosci 2004 27 307 340 15217335
- [2]Buhusi CV Meck WH What makes us tick? Functional and neural mechanisms of interval timing Nat Rev Neurosci 2005 6 755 765 16163383
- [3]Ivry RB Schlerf JE Dedicated and intrinsic models of time perception Trends in Cognitive Sciences 2008 12 273 280 18539519 PMC4335014
- [4]Church RM Meck WH Gibbon J Application of scalar timing theory to individual trials J Exp Psychol Anim Behav Process 1994 20 135 155 8189184
- [5]Durstewitz D Self-organizing neural integrator predicts interval times through climbing activity J Neurosci 2003 23 5342 5353 12832560 PMC6741165
- [6]Simen P Balci F de Souza L Cohen JD Holmes P A model of interval timing by neural integration J Neurosci 2011 31 9238 9253 21697374 PMC3142662
- [8]Matell MS Meck WH Nicolelis MA Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons Behav Neurosci 2003 117 760 773 12931961
- [9]Ahrens MB Sahani M Observers Exploit Stochastic Models of Sensory Change to Help Judge the Passage of Time Current Biology 2011 21 200 206 21256018 PMC3094759
- [10]Buonomano DV Laje R Population clocks: motor timing with neural dynamics Trends in Cognitive Sciences 2010 14 520 527 20889368 PMC2991437
- [11]Medina JF Mauk MD Computer simulation of cerebellar information processing Nat Neurosci 2000 3 Suppl 1205 1211 11127839
- [13]Buonomano DV Merzenich MM Temporal information transformed into a spatial code by a neural network with realistic properties Science 1995 267 1028 1030 7863330
- [14]Durstewitz D Deco G Computational significance of transient dynamics in cortical networks European Journal of Neuroscience 2008 27 217 227 18093174
- [15]Rabinovich M Huerta R Laurent G Transient Dynamics for Neural Processing Science 2008 321 48 50 18599763
- [16]Buonomano DV Maass W State-dependent Computations: Spatiotemporal Processing in Cortical Networks Nat Rev Neurosci 2009 10 113 125 19145235
- [17]Hahnloser RHR Kozhevnikov AA Fee MS An ultra-sparse code underlies the generation of neural sequence in a songbird Nature 2002 419 65 70 12214232
- [18]Long MA Jin DZ Fee MS Support for a synaptic chain model of neuronal sequence generation Nature 2010 468 394 399 20972420 PMC2998755
- [19]Crowe DA Averbeck BB Chafee MV Rapid Sequences of Population Activity Patterns Dynamically Encode Task-Critical Spatial Information in Parietal Cortex J. Neurosci 2010 30 11640 11653 20810885 PMC3020896
- [20]Li JX Lisberger SG Learned Timing of Motor Behavior in the Smooth Eye Movement Region of the Frontal Eye Fields Neuron 2011 69 159 169 21220106 PMC3063556
- [21]London M Roth A Beeren L Hausser M Latham PE Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex Nature 2010 466 123 127 20596024 PMC2898896
- [22]Izhikevich EM Edelman GM Large-scale model of mammalian thalamocortical systems Proc Natl Acad Sci U S A 2008 105 3593 3598 18292226 PMC2265160
- [23]van Vreeswijk C Sompolinsky H Chaos in neuronal networks with balanced excitatory and inhibitory activity Science 1996 274 1724 1726 8939866
- [24]Brunel N Dynamics of networks of randomly connected excitatory and inhibitory spiking neurons Journal of Physiology-Paris 2000 94 445 463 11165912
- [25]Banerjee A Series P Pouget A Dynamical constraints on using precise spike timing to compute in recurrent cortical networks Neural Comput 2008 20 974 993 18085984
- [26]Sompolinsky H Crisanti A Sommers HJ Chaos in random neural networks Physical Rev. Let 1988 61 259 262 10039285
- [27]Monteforte M Wolf F Dynamic Flux Tubes Form Reservoirs of Stability in Neuronal Circuits Physical Review X 2012 2 041007
- [29]Sussillo D Abbott LF Generating Coherent Patterns of Activity from Chaotic Neural Networks Neuron 2009 63 544 557 19709635 PMC2756108
- [30]Rajan K Abbott LF Sompolinsky H Stimulus-dependent suppression of chaos in recurrent neural networks Physical Rev. E 2010 82 011903(011905) PMC10683875 20866644
- [31]Doya K Circuits and Systems, 1992. ISCAS '92. Proceedings., 1992 IEEE International Symposium on 2776 2777 2780
- [33]Ganguli S Huh D Sompolinsky H Memory traces in dynamical systems Proceedings of the National Academy of Sciences 2008 PMC2596211 19020074
- [36]Watts DJ Strogatz SH Collective dynamics of `small-world’ networks Nature 1998 393 440 442 9623998
- [37]Janssen P Shadlen MN A representation of the hazard rate of elapsed time in the macaque area LIP Nat. Neurosci 2005 8 234 241 15657597
- [38]Bueti D Lasaponara S Cercignani M Macaluso E Learning about Time: Plastic Changes and Interindividual Brain Differences Neuron 2012 75 725 737 22920262
- [39]Coull J Nobre A Dissociating explicit timing from temporal expectation with fMRI Curr Opin Neurobiol 2008 18 137 144 18692573
- [40]Merchant H Zarco W Pérez O Prado L Bartolo R Measuring time with different neural chronometers during a synchronization-continuation task Proceedings of the National Academy of Sciences 2011 108 19784 19789 PMC3241773 22106292
- [41]Pastalkova E Itskov V Amarasingham A Buzsaki G Internally Generated Cell Assembly Sequences in the Rat Hippocampus Science 2008 321 1322 1327 18772431 PMC2570043
- [42]Ivry RB Keele SW Diener HC Dissociation of the lateral and medial cerebellum in movement timing and movement execution Exp. Brain Res 1988 73 167 180 3208855
- [43]Medina JF Garcia KS Nores WL Taylor NM Mauk MD Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation J Neurosci 2000 20 5516 5525 10884335 PMC6772322
- [44]Buonomano DV Decoding temporal information: a model based on short-term synaptic plasticity J Neurosci 2000 20 1129 1141 10648718 PMC6774169
- [45]Litwin-Kumar A Doiron B Slow dynamics and high variability in balanced cortical networks with clustered connections Nat Neurosci 2012 15 1498 1505 23001062 PMC4106684
- [46]Liu JK Buonomano DV Embedding Multiple Trajectories in Simulated Recurrent Neural Networks in a Self-Organizing Manner J. Neurosci 2009 29 13172 13181 19846705 PMC6665184
- [47]Goldman MS Memory without Feedback in a Neural Network Neuron 2009 61 621 634 19249281 PMC2674525
- [48]Hopfield JJ Neural networks and physical systems with emergent collective computational abilities Proc Natl Acad Sci U S A 1982 79 2554 2558 6953413 PMC346238
- [49]Wang XJ Synaptic reverberation underlying mnemonic persistent activity Trends Neurosci 2001 24 455 463 11476885
- [52]Haykin S Adaptive Filter Theory 2002 Prentice Hall
- [54]Boffetta G Lacorata G Radaelli G Vulpiani A Detecting barriers to transport: a review of different techniques Physica D 2001 159 58 70
- [55]Fagiolo G Clustering in complex directed networks Physical Review E 2007 76 17930104
Cited by
Sorted by citations
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
A neural network that finds a naturalistic solution for the production of muscle activity
Sussillo, D., Churchland, M. M., Kaufman, M. T., & Shenoy, K. V. (2015) · Nature Neuroscience · doi:10.1038/nn.4042 · Cited by 598 · see citing works
Robust neuronal dynamics in premotor cortex during motor planning
Li, N., Daie, K., Svoboda, K., & Druckmann, S. (2016) · Nature · doi:10.1038/nature17643 · Cited by 492 · see citing works
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
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
Harnessing Disordered-Ensemble Quantum Dynamics for Machine Learning
Fujii, K., & Nakajima, K. (2017) · Physical Review Applied · doi:10.1103/physrevapplied.8.024030 · Cited by 337 · see citing works
Song, H. F., Yang, G. R., & Wang, X.-J. (2016) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1004792 · Cited by 281 · see citing works
Neural circuits as computational dynamical systems
Sussillo, D. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.01.008 · Cited by 247 · see citing works
Flexible multitask computation in recurrent networks utilizes shared dynamical motifs
Driscoll, L., Shenoy, K., & Sussillo, D. (2022) · doi:10.1101/2022.08.15.503870 · Cited by 217 · see citing works
The Cerebro-Cerebellum as a Locus of Forward Model: A Review
Tanaka, H., Ishikawa, T., Lee, J., & Kakei, S. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.00019 · Cited by 155 · see citing works
Trujillo, C. A., Adams, J. W., Negraes, P. D., Carromeu, C., Tejwani, L., Acab, A., Tsuda, B., Thomas, C. A., Sodhi, N., Fichter, K. M., et al. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.202012523 · Cited by 101 · see citing works
Initial-state-dependent, robust, transient neural dynamics encode conscious visual perception
Baria, A. T., Maniscalco, B., & He, B. J. (2017) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1005806 · Cited by 70 · see citing works
Neurally Encoding Time for Olfactory Navigation
Park, I. J., Hein, A. M., Bobkov, Y. V., Reidenbach, M. A., Ache, B. W., & Principe, J. C. (2016) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1004682 · Cited by 50 · see citing works
- Authors
- Laje, R., & Buonomano, D. V.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Buonomano, Dean V
- Venue
- Nature Neuroscience
- Published
- 2013-05-26
- Volume
- 16
- Issue
- 7
- Pages
- 925-933
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3753043
- OpenAlex
- W1661597557
- Cited by
- 454
- References
- 3
- Citations by year
- 2026: 27 · 2025: 33 · 2024: 28 · 2023: 49 · 2022: 39 · 2021: 37 · 2020: 40 · 2019: 43 · 2018: 33 · 2017: 39 · 2016: 45 · 2015: 21 · 2014: 16 · 2013: 4
- FWCI
- 14.09
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- arXiv (Cornell University) (submittedVersion)
- CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
- Funders
- National Science Foundation (1114833, MH60163)
- Consejo Nacional de Investigaciones Científicas y Técnicas
- National Institute of Mental Health (MH-60163)
- National Institute of Neurological Disorders and Stroke (R03NS077340, NS077340)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Computer Science › Artificial Intelligence › Neural Networks and Applications
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Chaos control and synchronization
- Keywords
- recurrent neural networks, timekeeping, chaos, noise robustness, firing rate model, dynamic attractors, chaotic dynamics, perturbation stability, biological timekeeping
- MeSH terms
- Action Potentials, Animals, Computer Simulation, Humans, Learning, Models, Neurological, Motor Activity, Nerve Net, Neurons, Synapses, Time Perception, Nonlinear Dynamics
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