Long-term stability of cortical population dynamics underlying consistent behavior

Animals readily execute learned behaviors in a consistent manner over long periods of time, and yet no equally stable neural correlate has been demonstrated. How does the cortex achieve this stable control? Using the sensorimotor system as a model of cortical processing, we investigated the hypothesis that the dynamics of neural latent activity, which captures the dominant co-variation patterns within the neural population, must be preserved across time. We recorded from populations of neurons in premotor, primary motor and somatosensory cortices as monkeys performed a reaching task, for up to 2 years. Intriguingly, despite a steady turnover in the recorded neurons, the low-dimensional latent dynamics remained stable. The stability allowed reliable decoding of behavioral features for the entire timespan, while fixed decoders based directly on the recorded neural activity degraded substantially. We posit that stable latent cortical dynamics within the manifold are the fundamental building blocks underlying consistent behavioral execution. Gallego, Perich et al. report that latent dynamics in the neural manifold across three cortical areas are stable throughout years of consistent behavior. The authors posit that these dynamics are fundamental building blocks of learned behavior.

[1]  Lee E. Miller,et al.  A Neural Population Mechanism for Rapid Learning , 2017, Neuron.

[2]  Stephen I. Ryu,et al.  Leveraging neural dynamics to extend functional lifetime of brain-machine interfaces , 2017, Scientific Reports.

[3]  Christian Ethier,et al.  Cortical population activity within a preserved neural manifold underlies multiple motor behaviors , 2018, Nature Communications.

[4]  Byron M. Yu,et al.  Factor-analysis methods for higher-performance neural prostheses. , 2009, Journal of neurophysiology.

[5]  Yoshua Bengio,et al.  Adversarial Domain Adaptation for Stable Brain-Machine Interfaces , 2018, ICLR.

[6]  Jose M. Carmena,et al.  Closed-Loop Decoder Adaptation Shapes Neural Plasticity for Skillful Neuroprosthetic Control , 2014, Neuron.

[7]  Byron M. Yu,et al.  New neural activity patterns emerge with long-term learning , 2019, Proceedings of the National Academy of Sciences.

[8]  Hugo L. Fernandes,et al.  Primary motor cortical discharge during force field adaptation reflects muscle-like dynamics. , 2013, Journal of neurophysiology.

[9]  Krishna V. Shenoy,et al.  Accurate Estimation of Neural Population Dynamics without Spike Sorting , 2019, Neuron.

[10]  L. Miller,et al.  Restoring sensorimotor function through intracortical interfaces: progress and looming challenges , 2014, Nature Reviews Neuroscience.

[11]  Francesca Mastrogiuseppe,et al.  Linking Connectivity, Dynamics, and Computations in Low-Rank Recurrent Neural Networks , 2017, Neuron.

[12]  E. Bizzi,et al.  Motor Learning with Unstable Neural Representations , 2007, Neuron.

[13]  M. M. Morrow,et al.  Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. , 2003, Journal of neurophysiology.

[14]  Gamaleldin F. Elsayed,et al.  Structure in neural population recordings: an expected byproduct of simpler phenomena? , 2017, Nature Neuroscience.

[15]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[16]  A. Schwartz,et al.  High-performance neuroprosthetic control by an individual with tetraplegia , 2013, The Lancet.

[17]  R L Sainburg,et al.  Control of limb dynamics in normal subjects and patients without proprioception. , 1995, Journal of neurophysiology.

[18]  Chethan Pandarinath,et al.  Neural population dynamics in human motor cortex during movements in people with ALS , 2015, eLife.

[19]  Naoshige Uchida,et al.  Demixed principal component analysis of neural population data , 2014, eLife.

[20]  Konrad Paul Kording,et al.  Single reach plans in dorsal premotor cortex during a two-target task , 2018, Nature Communications.

[21]  Byron M. Yu,et al.  Neural constraints on learning , 2014, Nature.

[22]  L. Miller,et al.  Restoration of grasp following paralysis through brain-controlled stimulation of muscles , 2012, Nature.

[23]  David Sussillo,et al.  Making brain–machine interfaces robust to future neural variability , 2016, Nature communications.

[24]  Matthew T. Kaufman,et al.  A neural network that finds a naturalistic solution for the production of muscle activity , 2015, Nature Neuroscience.

[25]  John P. Cunningham,et al.  Single-Neuron Stability during Repeated Reaching in Macaque Premotor Cortex , 2007, The Journal of Neuroscience.

[26]  Vikash Gilja,et al.  Long-term Stability of Neural Prosthetic Control Signals from Silicon Cortical Arrays in Rhesus Macaque Motor Cortex , 2010 .

[27]  Lee E Miller,et al.  Responses of somatosensory area 2 neurons to actively and passively generated limb movements. , 2013, Journal of neurophysiology.

[28]  Emil Wärnberg,et al.  Perturbing low dimensional activity manifolds in spiking neuronal networks , 2019, PLoS Comput. Biol..

[29]  Surya Ganguli,et al.  A theory of multineuronal dimensionality, dynamics and measurement , 2017, bioRxiv.

[30]  Matthew G Perich,et al.  Altered tuning in primary motor cortex does not account for behavioral adaptation during force field learning , 2017, Experimental Brain Research.

[31]  Marc W Slutzky,et al.  Statistical assessment of the stability of neural movement representations. , 2011, Journal of neurophysiology.

[32]  Yali Amit,et al.  Single-unit stability using chronically implanted multielectrode arrays. , 2009, Journal of neurophysiology.

[33]  John P. Cunningham,et al.  Gaussian-process factor analysis for low-dimensional single-trial analysis of neural population activity , 2008, NIPS.

[34]  Byron M. Yu,et al.  A high-performance brain–computer interface , 2006, Nature.

[35]  Michael I. Jordan,et al.  Kernel independent component analysis , 2003 .

[36]  S. Scott Optimal feedback control and the neural basis of volitional motor control , 2004, Nature Reviews Neuroscience.

[37]  Lee E Miller,et al.  Inferring functional connections between neurons , 2008, Current Opinion in Neurobiology.

[38]  Robert D Flint,et al.  Long-Term Stability of Motor Cortical Activity: Implications for Brain Machine Interfaces and Optimal Feedback Control , 2016, The Journal of Neuroscience.

[39]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[41]  A B Schwartz,et al.  Motor cortical representation of speed and direction during reaching. , 1999, Journal of neurophysiology.

[42]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[43]  Byron M. Yu,et al.  Neural Variability in Premotor Cortex Provides a Signature of Motor Preparation , 2006, The Journal of Neuroscience.

[44]  Chethan Pandarinath,et al.  Inferring single-trial neural population dynamics using sequential auto-encoders , 2017, Nature Methods.

[45]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[46]  Eva L. Dyer,et al.  A cryptography-based approach for movement decoding , 2016, Nature Biomedical Engineering.

[47]  John P. Cunningham,et al.  Behaviorally Selective Engagement of Short-Latency Effector Pathways by Motor Cortex , 2017, Neuron.

[48]  Lee E. Miller,et al.  Neural Manifolds for the Control of Movement , 2017, Neuron.

[49]  Surya Ganguli,et al.  Cortical layer–specific critical dynamics triggering perception , 2019, Science.

[50]  Devika Narain,et al.  Flexible Sensorimotor Computations through Rapid Reconfiguration of Cortical Dynamics , 2018, Neuron.

[51]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[52]  J. Cunningham,et al.  Different population dynamics in the supplementary motor area and motor cortex during reaching , 2018, Nature Communications.

[53]  Wei Wu,et al.  Real-Time Decoding of Nonstationary Neural Activity in Motor Cortex , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[54]  Jakob H. Macke,et al.  Extracting low-dimensional dynamics from multiple large-scale neural population recordings by learning to predict correlations , 2017, NIPS.

[55]  Paul Nuyujukian,et al.  A high performing brain–machine interface driven by low-frequency local field potentials alone and together with spikes , 2015, bioRxiv.

[56]  J. Kalaska,et al.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. , 1994, Journal of neurophysiology.