NMDA-driven dendritic modulation enables multitask representation learning in hierarchical sensory processing pathways

Significance In deep learning, the standard approach to accommodate changing task demands is to train new output layers on top of a common trunk network, and, if needed, to relearn synapses throughout the whole network. However, the brain appears to take a radically different strategy, as neurons in all processing layers are modulated by contextual information. We show that context-dependent dendritic afferents can powerfully modulate the neuronal output and that this modulation dynamically reshapes network function to solve new tasks, without adapting any feedforward synapses. We furthermore show that these dendritic modulations could underlie self-supervised learning of deep networks, without relying on the backpropagation of errors across the layers of the network.

[1]  Fabian A. Mikulasch,et al.  Where is the error? Hierarchical predictive coding through dendritic error computation , 2022, Trends in Neurosciences.

[2]  Blake A. Richards,et al.  A ternary neural code resolves error and sharpening signals , 2022, bioRxiv.

[3]  M. Larkum,et al.  The Guide to Dendritic Spikes of the Mammalian Cortex In Vitro and In Vivo , 2022, Neuroscience.

[4]  M. Rule,et al.  Self-healing codes: How stable neural populations can track continually reconfiguring neural representations , 2022, Proceedings of the National Academy of Sciences.

[5]  Lucas O. Souza,et al.  Avoiding Catastrophe: Active Dendrites Enable Multi-Task Learning in Dynamic Environments , 2021, Frontiers in Neurorobotics.

[6]  Yaroslav Felipe Kalle Kossio,et al.  Drifting assemblies for persistent memory: Neuron transitions and unsupervised compensation , 2020, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Larkum,et al.  Memories off the top of your head , 2021, Science.

[8]  W. Freiwald,et al.  A fast link between face perception and memory in the temporal pole , 2021, Science.

[9]  B. Rudy,et al.  Neocortical Layer 1: An Elegant Solution to Top-Down and Bottom-Up Integration. , 2021, Annual review of neuroscience.

[10]  Yazan N. Billeh,et al.  Survey of spiking in the mouse visual system reveals functional hierarchy , 2021, Nature.

[11]  Michael J. Goard,et al.  Stimulus-dependent representational drift in primary visual cortex , 2020, Nature Communications.

[12]  W. Gerstner,et al.  Local plasticity rules can learn deep representations using self-supervised contrastive predictions , 2020, NeurIPS.

[13]  Alon Rubin,et al.  Representational drift in the mouse visual cortex , 2020, Current Biology.

[14]  Richard Axel,et al.  Representational drift in primary olfactory cortex , 2020, Nature.

[15]  Fritjof Helmchen,et al.  Value-guided remapping of sensory cortex by lateral orbitofrontal cortex , 2020, Nature.

[16]  T. Lillicrap,et al.  Backpropagation and the brain , 2020, Nature Reviews Neuroscience.

[17]  Walter Senn,et al.  Data-driven reduction of dendritic morphologies with preserved dendro-somatic responses , 2020, bioRxiv.

[18]  Geoffrey E. Hinton,et al.  A Simple Framework for Contrastive Learning of Visual Representations , 2020, ICML.

[19]  A. Angelucci,et al.  Anatomy and Physiology of Macaque Visual Cortical Areas V1, V2, and V5/MT: Bases for Biologically Realistic Models. , 2020, Cerebral cortex.

[20]  Natalia Gimelshein,et al.  PyTorch: An Imperative Style, High-Performance Deep Learning Library , 2019, NeurIPS.

[21]  Pengfei Liu,et al.  Learning Sparse Sharing Architectures for Multiple Tasks , 2019, AAAI.

[22]  Jessica A. Cardin,et al.  Functional flexibility in cortical circuits , 2019, Current Opinion in Neurobiology.

[23]  M. Larkum,et al.  Perirhinal input to neocortical layer 1 controls learning , 2019, Science.

[24]  Elia Formisano,et al.  Cortical encoding of speech enhances task-relevant acoustic information , 2019, Nature Human Behaviour.

[25]  Anitha Pasupathy,et al.  Task Context Modulates Feature-Selective Responses in Area V4 , 2019, The Journal of Neuroscience.

[26]  Wulfram Gerstner,et al.  Biologically plausible deep learning - but how far can we go with shallow networks? , 2019, Neural Networks.

[27]  Marc-Oliver Gewaltig,et al.  Electrical Compartmentalization in Neurons. , 2019, Cell reports.

[28]  Yoshua Bengio,et al.  Dendritic cortical microcircuits approximate the backpropagation algorithm , 2018, NeurIPS.

[29]  Nathalie L. Rochefort,et al.  The Impact of Visual Cues, Reward, and Motor Feedback on the Representation of Behaviorally Relevant Spatial Locations in Primary Visual Cortex , 2018, Cell reports.

[30]  Craig G. Richter,et al.  Top-down beta oscillatory signaling conveys behavioral context in early visual cortex , 2018, Scientific Reports.

[31]  Troy W. Margrie,et al.  A Circuit for Integration of Head- and Visual-Motion Signals in Layer 6 of Mouse Primary Visual Cortex , 2018, Neuron.

[32]  Leland McInnes,et al.  UMAP: Uniform Manifold Approximation and Projection for Dimension Reduction , 2018, ArXiv.

[33]  Nicolas Y. Masse,et al.  Alleviating catastrophic forgetting using context-dependent gating and synaptic stabilization , 2018, Proceedings of the National Academy of Sciences.

[34]  Y. Kawaguchi Pyramidal Cell Subtypes and Their Synaptic Connections in Layer 5 of Rat Frontal Cortex , 2017, Cerebral cortex.

[35]  Jessica A. Cardin,et al.  Sensation during Active Behaviors , 2017, The Journal of Neuroscience.

[36]  Henry Markram,et al.  Timed Synaptic Inhibition Shapes NMDA Spikes, Influencing Local Dendritic Processing and Global I/O Properties of Cortical Neurons. , 2017, Cell reports.

[37]  Aaron C. Courville,et al.  FiLM: Visual Reasoning with a General Conditioning Layer , 2017, AAAI.

[38]  Selmaan N. Chettih,et al.  Dynamic Reorganization of Neuronal Activity Patterns in Parietal Cortex , 2017, Cell.

[39]  Sebastian Ruder,et al.  An Overview of Multi-Task Learning in Deep Neural Networks , 2017, ArXiv.

[40]  Gregory Cohen,et al.  EMNIST: an extension of MNIST to handwritten letters , 2017, CVPR 2017.

[41]  Timothy P Lillicrap,et al.  Towards deep learning with segregated dendrites , 2016, eLife.

[42]  Hassana K. Oyibo,et al.  Experience-dependent spatial expectations in mouse visual cortex , 2016, Nature Neuroscience.

[43]  Dario L Ringach,et al.  Enhanced Spatial Resolution During Locomotion and Heightened Attention in Mouse Primary Visual Cortex , 2016, The Journal of Neuroscience.

[44]  Konrad P. Körding,et al.  Toward an Integration of Deep Learning and Neuroscience , 2016, bioRxiv.

[45]  Craig G. Richter,et al.  Top-Down Beta Enhances Bottom-Up Gamma , 2016, The Journal of Neuroscience.

[46]  Ha Hong,et al.  Explicit information for category-orthogonal object properties increases along the ventral stream , 2016, Nature Neuroscience.

[47]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[48]  Wulfram Gerstner,et al.  Nonlinear Hebbian Learning as a Unifying Principle in Receptive Field Formation , 2016, PLoS Comput. Biol..

[49]  Johannes C. Dahmen,et al.  Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex , 2015, Nature Neuroscience.

[50]  Subutai Ahmad,et al.  Why Neurons Have Thousands of Synapses, a Theory of Sequence Memory in Neocortex , 2015, Front. Neural Circuits.

[51]  S. Manita,et al.  A Top-Down Cortical Circuit for Accurate Sensory Perception , 2015, Neuron.

[52]  Sergey Ioffe,et al.  Batch Normalization: Accelerating Deep Network Training by Reducing Internal Covariate Shift , 2015, ICML.

[53]  Jian Sun,et al.  Delving Deep into Rectifiers: Surpassing Human-Level Performance on ImageNet Classification , 2015, 2015 IEEE International Conference on Computer Vision (ICCV).

[54]  Jimmy Ba,et al.  Adam: A Method for Stochastic Optimization , 2014, ICLR.

[55]  Vinay Jayaram,et al.  Speech-specific tuning of neurons in human superior temporal gyrus. , 2014, Cerebral cortex.

[56]  P. Roelfsema,et al.  Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex , 2014, Proceedings of the National Academy of Sciences.

[57]  Ha Hong,et al.  Performance-optimized hierarchical models predict neural responses in higher visual cortex , 2014, Proceedings of the National Academy of Sciences.

[58]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[59]  Bartlett W. Mel,et al.  Mechanisms underlying subunit independence in pyramidal neuron dendrites , 2013, Proceedings of the National Academy of Sciences.

[60]  J. Schiller,et al.  Active properties of neocortical pyramidal neuron dendrites. , 2013, Annual review of neuroscience.

[61]  C. Gilbert,et al.  Top-down influences on visual processing , 2013, Nature Reviews Neuroscience.

[62]  Lacey J. Kitch,et al.  Long-term dynamics of CA1 hippocampal place codes , 2013, Nature Neuroscience.

[63]  M. Carandini,et al.  Inhibition dominates sensory responses in awake cortex , 2012, Nature.

[64]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[65]  Idan Segev,et al.  Principles Governing the Operation of Synaptic Inhibition in Dendrites , 2012, Neuron.

[66]  Georg B. Keller,et al.  Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse , 2012, Neuron.

[67]  Matthew W Self,et al.  Different glutamate receptors convey feedforward and recurrent processing in macaque V1 , 2012, Proceedings of the National Academy of Sciences.

[68]  N. Mesgarani,et al.  Selective cortical representation of attended speaker in multi-talker speech perception , 2012, Nature.

[69]  Honglak Lee,et al.  An Analysis of Single-Layer Networks in Unsupervised Feature Learning , 2011, AISTATS.

[70]  Henry Markram,et al.  Models of Neocortical Layer 5b Pyramidal Cells Capturing a Wide Range of Dendritic and Perisomatic Active Properties , 2011, PLoS Comput. Biol..

[71]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[72]  Yann LeCun,et al.  Convolutional networks and applications in vision , 2010, Proceedings of 2010 IEEE International Symposium on Circuits and Systems.

[73]  Alain Destexhe,et al.  Inhibitory “Noise” , 2010, Front. Cell. Neurosci..

[74]  R. Tibshirani,et al.  A penalized matrix decomposition, with applications to sparse principal components and canonical correlation analysis. , 2009, Biostatistics.

[75]  Guillermo Sapiro,et al.  Online dictionary learning for sparse coding , 2009, ICML '09.

[76]  Mounya Elhilali,et al.  Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields , 2009, Neuron.

[77]  Jackie Schiller,et al.  Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. , 2008, Journal of neurophysiology.

[78]  Paul A. Rhodes,et al.  The Properties and Implications of NMDA Spikes in Neocortical Pyramidal Cells , 2006, The Journal of Neuroscience.

[79]  Matthew E. Larkum,et al.  The GABAB1b Isoform Mediates Long-Lasting Inhibition of Dendritic Ca2+ Spikes in Layer 5 Somatosensory Pyramidal Neurons , 2006, Neuron.

[80]  Michael L. Hines,et al.  The NEURON Book , 2006 .

[81]  A. P. Bannister,et al.  Inter- and intra-laminar connections of pyramidal cells in the neocortex , 2005, Neuroscience Research.

[82]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[83]  R. Goebel,et al.  Mirror-Symmetric Tonotopic Maps in Human Primary Auditory Cortex , 2003, Neuron.

[84]  Bartlett W. Mel,et al.  Pyramidal Neuron as Two-Layer Neural Network , 2003, Neuron.

[85]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[86]  J. Schiller,et al.  NMDA spikes in basal dendrites of cortical pyramidal neurons , 2000, Nature.

[87]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[88]  Stefan Rotter,et al.  Exact digital simulation of time-invariant linear systems with applications to neuronal modeling , 1999, Biological Cybernetics.

[89]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[90]  Erkki Oja,et al.  Principal components, minor components, and linear neural networks , 1992, Neural Networks.

[91]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[92]  CE Jahr,et al.  A quantitative description of NMDA receptor-channel kinetic behavior , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  Geoffrey E. Hinton,et al.  Learning representations by back-propagating errors , 1986, Nature.

[94]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[95]  Marc Parizeau,et al.  DEAP: evolutionary algorithms made easy , 2012, J. Mach. Learn. Res..

[96]  Alex Krizhevsky,et al.  Learning Multiple Layers of Features from Tiny Images , 2009 .

[97]  S. Gerber,et al.  Unsupervised Natural Experience Rapidly Alters Invariant Object Representation in Visual Cortex , 2008 .

[98]  J. Charles,et al.  A Sino-German λ 6 cm polarization survey of the Galactic plane I . Survey strategy and results for the first survey region , 2006 .

[99]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.