Coupled Hebbian learning and evolutionary dynamics in a formal model for structural synaptic plasticity

Theoretical models of neuronal function consider different mechanisms through which networks learn, classify and discern inputs. A central focus of these models is to understand how associations are established amongst neurons, in order to predict spiking patterns that are compatible with empirical observations. Although these models have led to major insights and advances, they still do not account for the astonishing velocity with which the brain solves certain problems and what lies behind its creativity, amongst others features. We examine two important components that may crucially aid comprehensive understanding of said neurodynamical processes. First, we argue that once presented with a problem, different putative solutions are generated in parallel by different groups or local neuronal complexes, with the subsequent stabilization and spread of the best solutions. Using mathematical models we show that this mechanism accelerates finding the right solutions. This formalism is analogous to standard replicator-mutator models of evolution where mutation is analogous to the probability of neuron state switching (on/off). The second factor that we incorporate is structural synaptic plasticity, i.e. the making of new and disbanding of old synapses, which we apply as a dynamical reorganization of synaptic connections. We show that Hebbian learning alone does not suffice to reach optimal solutions. However, combining it with parallel evaluation and structural plasticity opens up possibilities for efficient problem solving. In the resulting networks, topologies converge to subsets of fully connected components. Imposing costs on synapses reduces the connectivity, although the number of connected components remains robust. The average lifetime of synapses is longer for connections that are established early, and diminishes with synaptic cost.

[1]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[2]  Markus Butz,et al.  Homeostatic structural plasticity increases the efficiency of small-world networks , 2014, Front. Synaptic Neurosci..

[3]  D. Chklovskii,et al.  Geometry and Structural Plasticity of Synaptic Connectivity , 2002, Neuron.

[4]  G. Tononi An information integration theory of consciousness , 2004, BMC Neuroscience.

[5]  G. Knott,et al.  Formation of Dendritic Spines with GABAergic Synapses Induced by Whisker Stimulation in Adult Mice , 2002, Neuron.

[6]  P S Goldman-Rakic,et al.  Synaptogenesis in the prefrontal cortex of rhesus monkeys. , 1994, Cerebral cortex.

[7]  Edmund T. Rolls,et al.  Advantages of dilution in the connectivity of attractor networks in the brain , 2012, BICA 2012.

[8]  Eörs Szathmáry,et al.  Natural Selection in the Brain , 2010 .

[9]  W. Wildman,et al.  Theoretical Neuroscience , 2014 .

[10]  Arjen van Ooyen,et al.  Homeostatic structural plasticity can account for topology changes following deafferentation and focal stroke , 2014, Front. Neuroanat..

[11]  David J. C. MacKay,et al.  Information Theory, Inference, and Learning Algorithms , 2004, IEEE Transactions on Information Theory.

[12]  P. Husbands,et al.  Evolvable Neuronal Paths: A Novel Basis for Information and Search in the Brain , 2011, PloS one.

[13]  Eörs Szathmáry,et al.  Selectionist and Evolutionary Approaches to Brain Function: A Critical Appraisal , 2012, Front. Comput. Neurosci..

[14]  N. Toni,et al.  LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite , 1999, Nature.

[15]  H. Seung,et al.  Learning in Spiking Neural Networks by Reinforcement of Stochastic Synaptic Transmission , 2003, Neuron.

[16]  S. Wright,et al.  The shifting balance theory and macroevolution. , 1982, Annual review of genetics.

[17]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[18]  J. Changeux Neuronal man : the biology of mind , 1985 .

[19]  Noah D. Goodman,et al.  Theory learning as stochastic search in the language of thought , 2012 .

[20]  R. Buerger The Mathematical Theory of Selection, Recombination, and Mutation , 2000 .

[21]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[22]  Michael P. Kilgard,et al.  Harnessing plasticity to understand learning and treat disease , 2012, Trends in Neurosciences.

[23]  Charles Kemp,et al.  The discovery of structural form , 2008, Proceedings of the National Academy of Sciences.

[24]  Christian Tetzlaff,et al.  The formation of multi-synaptic connections by the interaction of synaptic and structural plasticity and their functional consequences , 2014, BMC Neuroscience.

[25]  Eörs Szathmáry,et al.  The Neuronal Replicator Hypothesis , 2010, Neural Computation.

[26]  E. Stengel,et al.  Biology of Mind , 1965 .

[27]  M. Kimura,et al.  An introduction to population genetics theory , 1971 .

[28]  N. Kasthuri,et al.  Long-term dendritic spine stability in the adult cortex , 2002, Nature.

[29]  Chrisantha Fernando,et al.  Copying and Evolution of Neuronal Topology , 2008, PloS one.

[30]  Chrisantha Fernando,et al.  Chemical, Neuronal, and Linguistic Replicators , 2009 .

[31]  J. Weeks An introduction to population , 2012 .

[32]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[33]  D. Purves,et al.  Changes in the dendritic branching of adult mammalian neurones revealed by repeated imaging in situ , 1985, Nature.

[34]  J. Changeux,et al.  A theory of the epigenesis of neuronal networks by selective stabilization of synapses. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Lund,et al.  A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys , 1979, The Journal of comparative neurology.

[36]  Sean L. Hill,et al.  Statistical connectivity provides a sufficient foundation for specific functional connectivity in neocortical neural microcircuits , 2012, Proceedings of the National Academy of Sciences.

[37]  William B. Levy Contrasting rules for synaptogenesis, modification of existing synapses, and synaptic removal as a function of neuronal computation , 2004, Neurocomputing.

[38]  Xiaohui Xie,et al.  Learning Curves for Stochastic Gradient Descent in Linear Feedforward Networks , 2003, Neural Computation.

[39]  G. Edelman Neural Darwinism: The Theory Of Neuronal Group Selection , 1989 .

[40]  F. Wörgötter,et al.  Activity-dependent structural plasticity , 2009, Brain Research Reviews.

[41]  H. Markram,et al.  Spontaneous and evoked synaptic rewiring in the neonatal neocortex , 2006, Proceedings of the National Academy of Sciences.

[42]  Reinhard Bürger,et al.  THE MUTATION MATRIX AND THE EVOLUTION OF EVOLVABILITY , 2007, Evolution; international journal of organic evolution.

[43]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.

[44]  Kerstin M. Mueller Neural Darwinism The Theory Of Neuronal Group Selection , 2016 .

[45]  Ananya Chowdhury,et al.  Synapse rearrangements upon learning: from divergent–sparse connectivity to dedicated sub-circuits , 2014, Trends in Neurosciences.

[46]  Bartlett W. Mel,et al.  Cortical rewiring and information storage , 2004, Nature.