A stable, long - term cortical signature underlying consistent behavior

Animals readily execute learned motor behaviors in a consistent manner over long periods of time, yet similarly stable neural correlates remained elusive up to now. 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 capture the dominant co-variation patterns within the neural population, are preserved across time. We recorded from populations of neurons in premotor, primary motor, and somatosensory cortices for up to two years as monkeys performed a reaching task. Intriguingly, despite steady turnover in the recorded neurons, the low-dimensional latent dynamics remained stable. Such stability allowed reliable decoding of behavioral features for the entire timespan, while fixed decoders based on the recorded neural activity degraded substantially. We posit that latent cortical dynamics within the manifold are the fundamental and stable building blocks underlying consistent behavioral execution.

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

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

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

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

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

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

[7]  Hong-Wei Xue,et al.  Arabidopsis PROTEASOME REGULATOR1 is required for auxin-mediated suppression of proteasome activity and regulates auxin signalling , 2016, Nature Communications.

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

[9]  K. Harris,et al.  Spontaneous Events Outline the Realm of Possible Sensory Responses in Neocortical Populations , 2009, Neuron.

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

[11]  S. Meagher Instant neural control of a movement signal , 2002 .

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

[13]  Surya Ganguli,et al.  On simplicity and complexity in the brave new world of large-scale neuroscience , 2015, Current Opinion in Neurobiology.

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

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

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

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

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

[19]  Christian K. Machens,et al.  Behavioral / Systems / Cognitive Functional , But Not Anatomical , Separation of “ What ” and “ When ” in Prefrontal Cortex , 2009 .

[20]  Kenneth D. Harris,et al.  High-dimensional geometry of population responses in visual cortex , 2019, Nat..

[21]  John P. Cunningham,et al.  Reorganization between preparatory and movement population responses in motor cortex , 2016, Nature Communications.

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

[23]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.

[24]  Lee E. Miller,et al.  A neural population mechanism for rapid learning , 2017 .

[25]  M. Sahani,et al.  Cortical control of arm movements: a dynamical systems perspective. , 2013, Annual review of neuroscience.

[26]  T. Lillicrap,et al.  Preference Distributions of Primary Motor Cortex Neurons Reflect Control Solutions Optimized for Limb Biomechanics , 2013, Neuron.

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

[28]  Markus Siegel,et al.  Cortical information flow during flexible sensorimotor decisions , 2015, Science.

[29]  D R Humphrey,et al.  Predicting Measures of Motor Performance from Multiple Cortical Spike Trains , 1970, Science.

[30]  Matthew T. Kaufman,et al.  A category-free neural population supports evolving demands during decision-making , 2014, Nature Neuroscience.

[31]  D. J. Weber,et al.  Limb-State Information Encoded by Peripheral and Central Somatosensory Neurons: Implications for an Afferent Interface , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[32]  Christopher I. Petkov,et al.  Complex Spectral Interactions Encoded by Auditory Cortical Neurons: Relationship Between Bandwidth and Pattern , 2010, Front. Syst. Neurosci..

[33]  L. Miller,et al.  Brain-controlled neuromuscular stimulation to drive neural plasticity and functional recovery , 2015, Current Opinion in Neurobiology.

[34]  L. L. Porter,et al.  Organization and synaptic relationships of the projection from the primary sensory to the primary motor cortex in the cat , 1988, The Journal of comparative neurology.

[35]  Lee E. Miller,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

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

[37]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

[38]  Byron M. Yu,et al.  Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex , 2016, PLoS Comput. Biol..

[39]  Bruce G Cumming,et al.  Decision-related activity in sensory neurons: correlations among neurons and with behavior. , 2012, Annual review of 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]  Devika Narain,et al.  Flexible timing by temporal scaling of cortical responses , 2017, Nature Neuroscience.

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

[43]  W. T. Thach Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. , 1978, Journal of neurophysiology.

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

[45]  Matthew T. Kaufman,et al.  Supplementary materials for : Cortical activity in the null space : permitting preparation without movement , 2014 .

[46]  Alexander S. Ecker,et al.  Recording chronically from the same neurons in awake, behaving primates. , 2007, Journal of neurophysiology.

[47]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

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

[49]  G. E. Alexander,et al.  Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. , 1997, Journal of neurophysiology.

[50]  Nicolas Y. Masse,et al.  Reach and grasp by people with tetraplegia using a neurally controlled robotic arm , 2012, Nature.

[51]  Gopal Santhanam,et al.  Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. , 2006, Journal of neurophysiology.

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

[53]  Devika Narain,et al.  Flexible sensorimotor computations through rapid reconfiguration of cortical dynamics , 2018 .

[54]  J. Kalaska,et al.  Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. , 2005, Journal of neurophysiology.

[55]  Michael I. Jordan,et al.  Kernel independent component analysis , 2003, 2003 IEEE International Conference on Acoustics, Speech, and Signal Processing, 2003. Proceedings. (ICASSP '03)..

[56]  P. Dayan,et al.  A mathematical model explains saturating axon guidance responses to molecular gradients , 2016, eLife.

[57]  C. Curtis,et al.  Multiple component networks support working memory in prefrontal cortex , 2015, Proceedings of the National Academy of Sciences.

[58]  A. Pollard,et al.  Limb proportions show developmental plasticity in response to embryo movement , 2017, Scientific Reports.

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

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

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

[62]  Lee E. Miller,et al.  Multiple tasks viewed from the neural manifold: Stable control of varied behavior , 2017, bioRxiv.

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

[64]  Stephen H. Scott,et al.  A Functional Taxonomy of Bottom-Up Sensory Feedback Processing for Motor Actions , 2016, Trends in Neurosciences.

[65]  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.

[66]  Surya Ganguli,et al.  Accurate Estimation of Neural Population Dynamics without Spike Sorting , 2017, Neuron.

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

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

[69]  E. Fetz,et al.  Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. , 1980, Journal of neurophysiology.

[70]  E. Evarts RELATION OF DISCHARGE FREQUENCY TO CONDUCTION VELOCITY IN PYRAMIDAL TRACT NEURONS. , 1965, Journal of neurophysiology.

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

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

[73]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

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

[75]  Robert D Flint,et al.  Long term, stable brain machine interface performance using local field potentials and multiunit spikes , 2013, Journal of neural engineering.

[76]  Abigail A. Russo,et al.  Motor Cortex Embeds Muscle-like Commands in an Untangled Population Response , 2018, Neuron.

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

[78]  David P. Friedman,et al.  Thalamic input to areas 3a and 2 in monkeys. , 1981, Journal of neurophysiology.

[79]  E. Fetz,et al.  Direct control of paralyzed muscles by cortical neurons , 2008, Nature.

[80]  C Ghez,et al.  Proprioceptive control of interjoint coordination. , 1995, Canadian journal of physiology and pharmacology.

[81]  J. Kaas,et al.  The somatotopic organization of area 2 in macaque monkeys , 1985, The Journal of comparative neurology.

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

[83]  J. Kaas,et al.  Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: A correlative anatomical and electrophysiological study , 1986, The Journal of comparative neurology.

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

[85]  David W. Tank,et al.  Probing variability in a cognitive map using manifold inference from neural dynamics , 2018, bioRxiv.

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

[87]  Qin,et al.  A Brain–Spinal Interface Alleviating Gait Deficits after Spinal Cord Injury in Primates , 2017 .

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

[89]  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.

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

[91]  C. Ghez,et al.  Loss of proprioception produces deficits in interjoint coordination. , 1993, Journal of neurophysiology.