A Computational Role for Astrocytes in Memory

The neuronal paradigm of studying the brain has left us with limitations in both our understanding of how neurons process information to achieve biological intelligence and how such knowledge may be translated into artificial intelligence and its most brain-derived branch, neuromorphic computing. Overturning our fundamental assumptions of how the brain works, the recent exploration of astrocytes is revealing that these long-neglected brain cells dynamically regulate learning by interacting with neuronal activity at the synaptic level. Following recent experimental evidence, we designed an associative, Hopfield-type, neuronal-astrocytic network and analyzed the dynamics of the interaction between neurons and astrocytes. We show that astrocytes were sufficient to trigger transitions between learned memories in the neuronal component of the network. Further, we mathematically derived the timing of the transitions that was governed by the dynamics of the calcium-dependent slow-currents in the astrocytic processes. Overall, we provide a brain-morphic mechanism for sequence learning that is inspired by, and aligns with, recent experimental findings. To evaluate our model, we emulated astrocytic atrophy and showed that memory recall becomes significantly impaired after a critical point of affected astrocytes was reached. This brain-inspired and brain-validated approach supports our ongoing efforts to incorporate non-neuronal computing elements in neuromorphic information processing.

[1]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[2]  J. Meldolesi,et al.  Astrocytes, from brain glue to communication elements: the revolution continues , 2005, Nature Reviews Neuroscience.

[3]  Terrence C. Stewart,et al.  An adaptive spiking neural controller for flapping insect-scale robots , 2017, 2017 IEEE Symposium Series on Computational Intelligence (SSCI).

[4]  D. Attwell,et al.  Astrocyte calcium signaling: the third wave , 2016, Nature Neuroscience.

[5]  B. Barres The Mystery and Magic of Glia: A Perspective on Their Roles in Health and Disease , 2008, Neuron.

[6]  H Sompolinsky,et al.  Associative neural network model for the generation of temporal patterns. Theory and application to central pattern generators. , 1988, Biophysical journal.

[7]  Kouichi Sakurai,et al.  One Pixel Attack for Fooling Deep Neural Networks , 2017, IEEE Transactions on Evolutionary Computation.

[8]  Chris Eliasmith,et al.  A spiking neural model of adaptive arm control , 2016, Proceedings of the Royal Society B: Biological Sciences.

[9]  E. Benarroch,et al.  Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. , 2005, Mayo Clinic proceedings.

[10]  J Anthony Movshon,et al.  Putting big data to good use in neuroscience , 2014, Nature Neuroscience.

[11]  Ananthram Swami,et al.  The Limitations of Deep Learning in Adversarial Settings , 2015, 2016 IEEE European Symposium on Security and Privacy (EuroS&P).

[12]  Wofgang Maas,et al.  Networks of spiking neurons: the third generation of neural network models , 1997 .

[13]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[14]  Bruce L. McNaughton,et al.  Path integration and the neural basis of the 'cognitive map' , 2006, Nature Reviews Neuroscience.

[15]  Rodrigo Alvarez-Icaza,et al.  Neurogrid: A Mixed-Analog-Digital Multichip System for Large-Scale Neural Simulations , 2014, Proceedings of the IEEE.

[16]  Kanter,et al.  Temporal association in asymmetric neural networks. , 1986, Physical review letters.

[17]  David A. Williams The Elephant in the Room , 2011 .

[18]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Lauritzen,et al.  Rapid stimulus-evoked astrocyte Ca2+ elevations and hemodynamic responses in mouse somatosensory cortex in vivo , 2013, Proceedings of the National Academy of Sciences.

[20]  Gopalakrishnan Srinivasan,et al.  Training Deep Spiking Convolutional Neural Networks With STDP-Based Unsupervised Pre-training Followed by Supervised Fine-Tuning , 2018, Front. Neurosci..

[21]  Michael Chen,et al.  Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. , 2013, Cell stem cell.

[22]  G. Dallérac,et al.  Astrocytes as new targets to improve cognitive functions , 2016, Progress in Neurobiology.

[23]  Chris Eliasmith,et al.  A Unified Approach to Building and Controlling Spiking Attractor Networks , 2005, Neural Computation.

[24]  Lujo Bauer,et al.  Accessorize to a Crime: Real and Stealthy Attacks on State-of-the-Art Face Recognition , 2016, CCS.

[25]  F. Crick Neurobiology: Memory and molecular turnover , 1984, Nature.

[26]  Vladimir Ivanov,et al.  A Neural-Astrocytic Network Architecture: Astrocytic calcium waves modulate synchronous neuronal activity , 2018, Proceedings of the International Conference on Neuromorphic Systems.

[27]  N. Brunel,et al.  Astrocytes: Orchestrating synaptic plasticity? , 2015, Neuroscience.

[28]  Andrew S. Cassidy,et al.  Cognitive computing building block: A versatile and efficient digital neuron model for neurosynaptic cores , 2013, The 2013 International Joint Conference on Neural Networks (IJCNN).

[29]  W. Pitts,et al.  A Logical Calculus of the Ideas Immanent in Nervous Activity (1943) , 2021, Ideas That Created the Future.

[30]  Eshel Ben-Jacob,et al.  Nonlinear Gap Junctions Enable Long-Distance Propagation of Pulsating Calcium Waves in Astrocyte Networks , 2010, PLoS Comput. Biol..

[31]  A. Turing Intelligent Machinery, A Heretical Theory* , 1996 .

[32]  Ioannis Polykretis,et al.  The Astrocytic Microdomain as a Generative Mechanism for Local Plasticity , 2018, BI.

[33]  T. Sejnowski,et al.  Glial Biology in Learning and Cognition , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[34]  M. London,et al.  Astrocytic Activation Generates De Novo Neuronal Potentiation and Memory Enhancement , 2018, Cell.

[35]  Beth Stevens,et al.  Do glia drive synaptic and cognitive impairment in disease? , 2015, Nature Neuroscience.

[36]  A. Verkhratsky,et al.  Astrocytes in Alzheimer’s disease , 2010, Neurotherapeutics.

[37]  S. Gobbo,et al.  Neuronal Synchrony Mediated by Astrocytic Glutamate through Activation of Extrasynaptic NMDA Receptors , 2004, Neuron.

[38]  Michael M. Halassa,et al.  Synaptic Islands Defined by the Territory of a Single Astrocyte , 2007, The Journal of Neuroscience.

[39]  A. Araque,et al.  Tripartite synapses: glia, the unacknowledged partner , 1999, Trends in Neurosciences.

[40]  S. Oliet,et al.  Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. , 2008, Physiological reviews.

[41]  A. Compte,et al.  Bump attractor dynamics in prefrontal cortex explains behavioral precision in spatial working memory , 2014, Nature Neuroscience.

[42]  Kaushik Roy,et al.  Going Deeper in Spiking Neural Networks: VGG and Residual Architectures , 2018, Front. Neurosci..

[43]  Matthew Cook,et al.  Fast-classifying, high-accuracy spiking deep networks through weight and threshold balancing , 2015, 2015 International Joint Conference on Neural Networks (IJCNN).

[44]  Hong Wang,et al.  Loihi: A Neuromorphic Manycore Processor with On-Chip Learning , 2018, IEEE Micro.

[45]  Ohad Shamir,et al.  Distribution-Specific Hardness of Learning Neural Networks , 2016, J. Mach. Learn. Res..

[46]  J. Kelso,et al.  Bidirectional Coupling between Astrocytes and Neurons Mediates Learning and Dynamic Coordination in the Brain: A Multiple Modeling Approach , 2011, PloS one.

[47]  John von Neumann,et al.  The Computer and the Brain , 1960 .

[48]  B. Pál Astrocytic Actions on Extrasynaptic Neuronal Currents , 2015, Front. Cell. Neurosci..

[49]  P. Haydon,et al.  Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Michael M. Halassa,et al.  Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. , 2010, Annual review of physiology.

[51]  Mriganka Sur,et al.  Neuron-glia networks: integral gear of brain function , 2014, Front. Cell. Neurosci..

[52]  A. Araque,et al.  Endocannabinoids Potentiate Synaptic Transmission through Stimulation of Astrocytes , 2010, Neuron.

[53]  Peter Blouw,et al.  Benchmarking Keyword Spotting Efficiency on Neuromorphic Hardware , 2018, NICE '19.

[54]  Andrew S. Cassidy,et al.  A million spiking-neuron integrated circuit with a scalable communication network and interface , 2014, Science.

[55]  Rishidev Chaudhuri,et al.  Computational principles of memory , 2016, Nature Neuroscience.

[56]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

[57]  Vladimir Parpura,et al.  A possible role of astrocytes in contextual memory retrieval: An analysis obtained using a quantitative framework , 2013, Front. Comput. Neurosci..

[58]  Timothée Masquelier,et al.  Deep Learning in Spiking Neural Networks , 2018, Neural Networks.

[59]  Steve B. Furber,et al.  The SpiNNaker Project , 2014, Proceedings of the IEEE.

[60]  Johannes Schemmel,et al.  A wafer-scale neuromorphic hardware system for large-scale neural modeling , 2010, Proceedings of 2010 IEEE International Symposium on Circuits and Systems.

[61]  F ROSENBLATT,et al.  The perceptron: a probabilistic model for information storage and organization in the brain. , 1958, Psychological review.

[62]  Samy Bengio,et al.  Understanding deep learning requires rethinking generalization , 2016, ICLR.

[63]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[64]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Carver Mead,et al.  Analog VLSI and neural systems , 1989 .

[66]  Jeffrey L. Krichmar,et al.  A self-driving robot using deep convolutional neural networks on neuromorphic hardware , 2016, 2017 International Joint Conference on Neural Networks (IJCNN).