Synaptic organizations and dynamical properties of weakly connected neural oscillators

Abstract.We study weakly connected networks of neural oscillators near multiple Andronov-Hopf bifurcation points. We analyze relationships between synaptic organizations (anatomy) of the networks and their dynamical properties (function). Our principal assumptions are: (1) Each neural oscillatorcomprises two populations of neurons: excitatory and inhibitory ones; (2) activity of each population of neurons is described by a scalar (one-dimensional) variable; (3) each neural oscillatoris near a nondegenerate supercritical Andronov-Hopf bifurcation point; (4) the synaptic connections between the neural oscillatorsare weak. All neural networks satisfying these hypotheses are governed by the same dynamical system, which we call the canonical model. Studying the canonical model shows that: (1) A neural oscillatorcan communicate only with those oscillators which have roughly the same natural frequency. That is, synaptic connections between a pair of oscillators having different natural frequencies are functionally insignificant. (2) Two neural oscillatorshaving the same natural frequencies might not communicate if the connections between them are from among a class of pathological synaptic configurations. In both cases the anatomical presence of synaptic connections between neural oscillators does not necessarily guarantee that the connections are functionally significant. (3) There can be substantial phase differences (time delays) between the neural oscillators, which result from the synaptic organization of the network, not from the transmission delays. Using the canonical model we can illustrate self-ignition and autonomous quiescence (oscillator death) phenomena. That is, a network of passive elements can exhibit active properties and vice versa. We also study how Dale's principle affects dynamics of the networks, in particular, the phase differences that the network can reproduce. We present a complete classification of all possible synaptic organizations from this point of view. The theory developed here casts some light on relations between synaptic organization and functional properties of oscillatory networks. The major advantage of our approach is that we obtain results about all networks of neural oscillators, including the real brain. The major drawback is that our findings are valid only when the brain operates near a critical regime, viz. for a multiple Andronov-Hopf bifurcation.

[1]  Guenter W. Gross,et al.  Neuronal networks with spontaneous, correlated bursting activity: Theory and simulations , 1992, Neural Networks.

[2]  G. Ermentrout,et al.  Oscillator death in systems of coupled neural oscillators , 1990 .

[3]  K. Bar-Eli,et al.  On the stability of coupled chemical oscillators , 1985 .

[4]  F C Hoppensteadt,et al.  Intermittent chaos, self-organization, and learning from synchronous synaptic activity in model neuron networks. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[5]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[6]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[7]  W. Freeman,et al.  How brains make chaos in order to make sense of the world , 1987, Behavioral and Brain Sciences.

[8]  F C Hoppensteadt,et al.  The searchlight hypothesis , 1991, Journal of mathematical biology.

[9]  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.

[10]  Stephen Grossberg,et al.  Nonlinear neural networks: Principles, mechanisms, and architectures , 1988, Neural Networks.

[11]  H. Dale Pharmacology and Nerve-Endings , 1935 .

[12]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[13]  G. Ermentrout,et al.  Amplitude response of coupled oscillators , 1990 .

[14]  B. Baird Nonlinear dynamics of pattern formation and pattern recognition in the rabbit olfactory bulb , 1986 .

[15]  Michail Zak,et al.  Weakly connected neural nets , 1990 .

[16]  Bard Ermentrout,et al.  Learning of Phase Lags in Coupled Neural Oscillators , 1994, Neural Computation.

[17]  Frank C. Hoppensteadt,et al.  Synaptic organizations and dynamical properties of weakly connected neural oscillators II. Learning phase information , 1996, Biological Cybernetics.

[18]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[19]  Nancy Kopell,et al.  Coupled Oscillators and Locomotion by Fish , 1986 .

[20]  P. Rakić Local circuit neurons. , 1975, Neurosciences Research Program bulletin.

[21]  J. Neu Coupled Chemical Oscillators , 1979 .

[22]  Frank C. Hoppensteadt,et al.  Analysis and simulation of chaotic systems , 1992 .

[23]  Frank C. Hoppensteadt,et al.  Bifurcations in brain dynamics , 1996 .

[24]  V. I. Kryukov,et al.  An attention model based on the principle of dominanta , 1991 .