Synaptic Darwinism and neocortical function

Abstract We propose that certain brain systems, such as those of neocortex, exploit a fusion of ideas from neural networks and evolutionary computation, and that several previously puzzling features of thalamocortical circuitry and physiology can be understood as consequences of this fusion. The starting point is a consideration of anatomical errors in the recently described digital strengthening of synaptic connections, which are analogous to mutations. A mathematical model of this process shows the equivalence of the intrinsic error rate and a “correlation ratio” which reflects the spatial variation in the degree of synchrony of neural firing. The correlation ratio plays a similar role to fitness ratios in genetic algorithms. It is argued that a major trend in brain evolution has been decreases in the intrinsic error rate, allowing increases in circuit complexity, but that biophysical limits to this trend have forced the neocortex to adopt a virtual error-reduction strategy. This requires online measurement of correlation ratios and control of the plasticity of the connections formed by individual neurons.

[1]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

[2]  Moshe Sipper,et al.  An Introduction To Articial Life , 1995 .

[3]  M. Volkenstein,et al.  Physical Approaches to Biological Evolution , 1994 .

[4]  J. Rinzel,et al.  The role of dendrites in auditory coincidence detection , 1998, Nature.

[5]  W. Abraham,et al.  Metaplasticity: A new vista across the field of synaptic plasticity , 1997, Progress in Neurobiology.

[6]  C. Adami,et al.  Introduction To Artificial Life , 1997, IEEE Trans. Evol. Comput..

[7]  R. Guillery,et al.  Functional organization of thalamocortical relays. , 1996, Journal of neurophysiology.

[8]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[9]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[10]  R. Douglas,et al.  The role of synapses in cortical computation , 1996, Journal of neurocytology.

[11]  KD Miller.  A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[13]  A. Aertsen,et al.  Synaptic plasticity in rat hippocampal slice cultures: local "Hebbian" conjunction of pre- and postsynaptic stimulation leads to distributed synaptic enhancement. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[14]  F. Engert,et al.  Synapse specificity of long-term potentiation breaks down at short distances , 1997, Nature.

[15]  F. Morrell,et al.  Structural synaptic correlate of long‐term potentiation: Formation of axospinous synapses with multiple, completely partitioned transmission zones , 1993, Hippocampus.

[16]  Sun-Yuan Kung,et al.  Principal Component Neural Networks: Theory and Applications , 1996 .

[17]  J. Isaac,et al.  Evidence for silent synapses: Implications for the expression of LTP , 1995, Neuron.

[18]  L. Cook.  The Genetical Theory of Natural Selection — A Complete Variorum Edition , 2000, Heredity.

[19]  Eric R. Kandel,et al.  Recruitment of New Sites of Synaptic Transmission During the cAMP-Dependent Late Phase of LTP at CA3–CA1 Synapses in the Hippocampus , 1997, Neuron.

[20]  B. Sakmann,et al.  Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Joel L. Davis,et al.  An Introduction to Neural and Electronic Networks , 1995 .

[22]  C. Malsburg.  Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[23]  M. Eigen.  Selforganization of matter and the evolution of biological macromolecules , 1971, Naturwissenschaften.

[24]  Michael I. Jordan,et al.  A more biologically plausible learning rule for neural networks. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[25]  C. Koch,et al.  The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Alonso,et al.  Functional connectivity between simple cells and complex cells in cat striate cortex , 1998, Nature Neuroscience.

[27]  P Siekevitz,et al.  Plasticity in the central nervous system: do synapses divide? , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Hopfield,et al.  All-or-none potentiation at CA3-CA1 synapses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Kingsley J. A. Cox,et al.  Implications of synaptic digitisation and error for neocortical function , 2000, Neurocomputing.

[30]  E. G. Jones,et al.  Viewpoint: the core and matrix of thalamic organization , 1998, Neuroscience.

[31]  R. Axel,et al.  Odorant Receptors Govern the Formation of a Precise Topographic Map , 1998, Cell.

[32]  R. Llinás,et al.  Brainstem control of wakefulness and sleep, Steriade, McCarley. Plenum Press, New York (1990), Price $85.00 , 1991 .

[33]  D. Madison,et al.  Locally distributed synaptic potentiation in the hippocampus. , 1994, Science.

[34]  U. Frey,et al.  Chapter 6 - Cellular Mechanisms Of Long-Term Potentiation: Late Maintenance , 1997 .

[35]  Gail A. Carpenter,et al.  Self-organizing neural network architectures for real-time adaptive pattern recognition , 1990 .