Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons

It has been conjectured that nonlinear processing in dendritic branches endows individual neurons with the capability to perform complex computational operations that are needed to solve for example the binding problem. However, it is not clear how single neurons could acquire such functionality in a self-organized manner, because most theoretical studies of synaptic plasticity and learning concentrate on neuron models without nonlinear dendritic properties. In the meantime, a complex picture of information processing with dendritic spikes and a variety of plasticity mechanisms in single neurons has emerged from experiments. In particular, new experimental data on dendritic branch strength potentiation in rat hippocampus have not yet been incorporated into such models. In this article, we investigate how experimentally observed plasticity mechanisms, such as depolarization-dependent spike-timing-dependent plasticity and branch-strength potentiation, could be integrated to self-organize nonlinear neural computations with dendritic spikes. We provide a mathematical proof that, in a simplified setup, these plasticity mechanisms induce a competition between dendritic branches, a novel concept in the analysis of single neuron adaptivity. We show via computer simulations that such dendritic competition enables a single neuron to become member of several neuronal ensembles and to acquire nonlinear computational capabilities, such as the capability to bind multiple input features. Hence, our results suggest that nonlinear neural computation may self-organize in single neurons through the interaction of local synaptic and dendritic plasticity mechanisms.

[1]  Eric R Kandel,et al.  The Biology of Memory: A Forty-Year Perspective , 2009, The Journal of Neuroscience.

[2]  H. Dringenberg,et al.  Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. , 2006, Cerebral cortex.

[3]  A. Polsky,et al.  Synaptic Integration in Tuft Dendrites of Layer 5 Pyramidal Neurons: A New Unifying Principle , 2009, Science.

[4]  Matthew E Larkum,et al.  Synaptic clustering by dendritic signalling mechanisms , 2008, Current Opinion in Neurobiology.

[5]  W. Gerstner,et al.  Connectivity reflects coding: a model of voltage-based STDP with homeostasis , 2010, Nature Neuroscience.

[6]  Haim Sompolinsky,et al.  Learning Input Correlations through Nonlinear Temporally Asymmetric Hebbian Plasticity , 2003, The Journal of Neuroscience.

[7]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[8]  Bartlett W. Mel Why Have Dendrites? A Computational Perspective , 1999 .

[9]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  P. J. Sjöström,et al.  Dendritic excitability and synaptic plasticity. , 2008, Physiological reviews.

[11]  M. Häusser,et al.  Dendritic Discrimination of Temporal Input Sequences in Cortical Neurons , 2010, Science.

[12]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.

[13]  W. Abraham Metaplasticity: tuning synapses and networks for plasticity , 2008, Nature Reviews Neuroscience.

[14]  Wulfram Gerstner,et al.  Predicting spike timing of neocortical pyramidal neurons by simple threshold models , 2006, Journal of Computational Neuroscience.

[15]  A. Polsky,et al.  Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study , 2007, Nature Neuroscience.

[16]  Minija Tamosiunaite,et al.  Erratum to: Self-influencing synaptic plasticity: recurrent changes of synaptic weights can lead to specific functional properties , 2010, Journal of Computational Neuroscience.

[17]  John N. J. Reynolds,et al.  Dopamine-dependent plasticity of corticostriatal synapses , 2002, Neural Networks.

[18]  Nace L. Golding,et al.  Dendritic spikes as a mechanism for cooperative long-term potentiation , 2002, Nature.

[19]  S. Kelso,et al.  Hebbian synapses in hippocampus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Wulfram Gerstner,et al.  Intrinsic Stabilization of Output Rates by Spike-Based Hebbian Learning , 2001, Neural Computation.

[21]  J. Magee,et al.  Integrative Properties of Radial Oblique Dendrites in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[22]  W. Singer,et al.  Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex , 1992, Brain Research.

[23]  Nicolangelo Iannella,et al.  Synaptic efficacy cluster formation across the dendrite via STDP , 2006, Neuroscience Letters.

[24]  Q. Gu Contribution of acetylcholine to visual cortex plasticity , 2003, Neurobiology of Learning and Memory.

[25]  A. Artola,et al.  Synaptic Activity Modulates the Induction of Bidirectional Synaptic Changes in Adult Mouse Hippocampus , 2000, The Journal of Neuroscience.

[26]  M Segal,et al.  A novel cholinergic induction of long-term potentiation in rat hippocampus. , 1994, Journal of neurophysiology.

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

[28]  Minija Tamosiunaite,et al.  Self-influencing synaptic plasticity: Recurrent changes of synaptic weights can lead to specific functional properties , 2007, Journal of Computational Neuroscience.

[29]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[30]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[31]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[32]  Domenico Tegolo,et al.  Single neuron binding properties and the magical number 7 , 2008, Hippocampus.

[33]  Mark C. W. van Rossum,et al.  Memory retention and spike-timing-dependent plasticity. , 2009, Journal of neurophysiology.

[34]  Mark C. W. van Rossum,et al.  Stable Hebbian Learning from Spike Timing-Dependent Plasticity , 2000, The Journal of Neuroscience.

[35]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[36]  Eytan Domany,et al.  Models of Neural Networks I , 1991 .

[37]  P. E. Gold,et al.  Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[39]  Niraj S. Desai,et al.  Frontiers in Synaptic Neuroscience Synaptic Neuroscience , 2022 .

[40]  Kenji Morita Possible Role of Dendritic Compartmentalization in the Spatial Working Memory Circuit , 2008, The Journal of Neuroscience.

[41]  Judit K. Makara,et al.  Experience-dependent compartmentalized dendritic plasticity in rat hippocampal CA1 pyramidal neurons , 2009, Nature Neuroscience.

[42]  G. Stuart,et al.  Dependence of EPSP Efficacy on Synapse Location in Neocortical Pyramidal Neurons , 2002, Science.

[43]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[44]  Judit K. Makara,et al.  Compartmentalized dendritic plasticity and input feature storage in neurons , 2008, Nature.

[45]  Bartlett W. Mel,et al.  Information Processing in Dendritic Trees , 1994, Neural Computation.

[46]  N. Spruston,et al.  Synaptic Depolarization Is More Effective than Back-Propagating Action Potentials during Induction of Associative Long-Term Potentiation in Hippocampal Pyramidal Neurons , 2009, The Journal of Neuroscience.

[47]  A. Treisman The binding problem , 1996, Current Opinion in Neurobiology.

[48]  Marvin Minsky,et al.  Perceptrons: An Introduction to Computational Geometry , 1969 .

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

[50]  Bartlett W. Mel,et al.  Dendrites: bug or feature? , 2003, Current Opinion in Neurobiology.

[51]  L. Abbott,et al.  Limits on the memory storage capacity of bounded synapses , 2007, Nature Neuroscience.

[52]  Wulfram Gerstner,et al.  Spiking Neuron Models , 2002 .

[53]  Bartlett W. Mel,et al.  Capacity-Enhancing Synaptic Learning Rules in a Medial Temporal Lobe Online Learning Model , 2009, Neuron.

[54]  Karel Svoboda,et al.  Locally dynamic synaptic learning rules in pyramidal neuron dendrites , 2007, Nature.

[55]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[56]  R. Kempter,et al.  Hebbian learning and spiking neurons , 1999 .

[57]  Jozsef Csicsvari,et al.  Activity-Dependent Control of Neuronal Output by Local and Global Dendritic Spike Attenuation , 2009, Neuron.

[58]  B. Sakmann,et al.  Spine Ca2+ Signaling in Spike-Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[59]  William M. DeBello,et al.  Micro-rewiring as a substrate for learning , 2008, Trends in Neurosciences.

[60]  Nathalie L Rochefort,et al.  Dendritic organization of sensory input to cortical neurons in vivo , 2010, Nature.