2015 Special IssueMathematical modeling for evolution of heterogeneous modules in the brain
Introduction
Modular architecture is one of the most frequently referenced concepts of neural organization (Felleman and Van Essen, 1991, Mountcastle, 1997, Szentágothai, 1983). In biological systems, such modular architecture has been self-organized in ontogeny, influenced by phylogeny (Wagner, Pavlicev, & Cheverud, 2007). In contrast, the modules and their interactions of artificial machines are designed by humans. Understanding the mechanism giving rise to functionally differentiated modules in biological systems, such as cortical module architectures, is of great interest.
In theoretical studies, it has been proposed that maximizing information transmission between subsystems can be used as a guiding principle for understanding the development and evolution of complex brain networks. Linsker, 1988, Linsker, 1989, Linsker, 1997 shows that information transmission between successive layers of feed-forward networks is a viable principle for designing functional neural networks. Recently, Tanaka, Kaneko, and Aoyagi (2009) showed that the learning algorithm that maximizes information retention in recurrent networks also gives rise to the appearance of biological structures, such as cell assemblies, and even to dynamics, such as spontaneous activity of synfire chain and critical neuronal avalanches. One of the present authors has proposed the idea of a new self-organization principle based on a variational principle (Kaneko and Tsuda, 2001, Tsuda, 1984, Tsuda, 2001): components (or elements) are self-organized according to constraints that act on the whole system, whereas according to the usual self-organization principles (ex. Haken, 1980, Nicolis and Prigogine, 1977), macroscopic order is self-organized via interactions among microscopic elements. Actually, neuron-like elements as components of a system have been obtained under the condition of maximum transmission of information across a whole system (Ito and Tsuda, 2007, Watanabe et al., in preparation). In the brain, bidirectional information transmission among modules is crucial for information processing. In fact, most connections between cortical modules are known to be bidirectional (Felleman & Van Essen, 1991). Yamaguti, Tsuda, and Takahashi (2014) have found intermittent switching of direction of information flow in two heterogeneously coupled chaotic systems. Such a mechanism may be applicable to bidirectional information transmission in neural systems.
Motivated by these studies, here we propose a mathematical model for functional differentiation induced by selection based on maximizing bidirectional information transmission. We try to extract the essence of evolutionary dynamics by investigating a coupled-oscillator network model. We construct randomly coupled-oscillator networks, each consisting of two sub-networks, by using a discretized version of the Kuramoto phase oscillator model (Kuramoto, 1984). Each sub-network consists of oscillators, whose states are represented by phase variables. A genetic algorithm is used to modify the parameters to the direction of better fitness. Transfer entropy (Schreiber, 2000), which measures directed information transfer, is estimated to quantify information flow between the two sub-networks in both directions and their product is regarded as fitness in the evolutionary process.
In Section 2, the proposed network model, analytic method, and procedure for evolution by the genetic algorithm are described. In Section 3, we give numerical results of this evolutionary process. In Section 4, we study the fitness landscape around the optimum network, exploring the parameter space as a means of characterizing the evolutionary process from the viewpoint of dynamical systems. In Section 5, dependences of the coupling density on heterogeneity are investigated. Section 6 is devoted to summary and discussions.
Section snippets
Network model
We consider a network of oscillators, which consists of two sub-network systems. Each sub-network consists of phase oscillators, whose dynamics is described by a discrete-time version of the Kuramoto model (Barlev et al., 2010, Daido, 1986, Kuramoto, 1984). It is known that the dynamics of weakly coupled oscillators that have stable limit-cycles can be reduced to a coupled equation of phase oscillators by using a reduction technique (Kuramoto, 1984). The Kuramoto model corresponds to the
Evolution of the network
We numerically simulated network evolution. In this section, the result for is shown. By the end of simulation (1000 generations), the mean fitness of the selected networks was almost saturated (Fig. 2(A)). In all simulations, genome populations were distributed around their mean values in a single cluster; split populations were not observed at the end of the evolution. The parameter values of the network at the end of the evolution and its schematic diagram are summarized in Fig. 2.
Fitness landscape around the optimized network
In this section, we explored the fitness landscape around the network with the optimal parameters found in the previous section. We investigate landscapes of two-dimensional spaces spanned by two control parameters, fixing other parameters in the vicinity of optimal values.
Fig. 5(A) shows the fitness landscape of parameter space, where . Other parameter values are fixed as follows: , , , and . Fig. 5(B) shows means and standard
Dependence on structural inhomogeneity
How does the emergence of heterogeneous modules depend on the coupling density? In this section, we investigate the dependence of the emergence of heterogeneous modules on sparseness of couplings.
Discussion
Development of two interacting sub-networks by an evolutionary algorithm under the constraint of maximizing bidirectional information transmission was studied. Emergence of differentiated modules was demonstrated. By exploring the parameter space of the network around the optimum set of parameter values, it was found that optimal networks exist near transition points, at which the incoherent state loses its stability and an extremely slow oscillatory behavior emerges. Our results support the
Acknowledgments
This work was partially supported by a Grant-in-Aid for Scientific Research on Innovative Areas “The study on the neural dynamics for understanding communication in terms of complex hetero systems (No. 4103)” (21120002) of the Ministry of Education, Culture, Sports, Science and Technology, Japan, by the Human Frontier Science Program (RGP0039/2010), and by JSPS KAKENHI Grant (No. 26540123). The authors would like to thank the anonymous reviewers for giving valuable comments that improved this
References (40)
- et al.
Analysing connectivity with Granger causality and dynamic causal modelling
Current Opinion in Neurobiology
(2013) - et al.
Information transfer in continuous processes
Physica D
(2002) - et al.
Rhythmic modulation of theta oscillations supports encoding of spatial and behavioral information in the rat hippocampus
Neuron
(2012) - et al.
Map model for synchronization of systems of many coupled oscillators
Chaos
(2010) Granger causality and transfer entropy are equivalent for Gaussian variables
Physical Review Letters
(2009)- et al.
An information-maximization approach to blind separation and blind deconvolution
Neural Computing
(1995) - et al.
Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality
Proceedings of the National Academy of Sciences of the United States of America
(2004) - et al.
The evolutionary origins of modularity
Proceedings of the Royal Society B: Biological Sciences
(2013) Discrete-time population dynamics of interacting self-oscillators
Progress of Theoretical Physics
(1986)- et al.
Specialization can drive the evolution of modularity
PLoS Computational Biology
(2010)
Distributed hierarchical processing in the primate cerebral cortex
Cerebral Cortex
The human brain is intrinsically organized into dynamic, anticorrelated functional networks
Proceedings of the National Academy of Sciences of the United States of America
Investigating causal relations by econometric models and cross-spectral methods
Econometrica: Journal of the Econometric Society
Synergetics
Naturwissenschaften
Adaptation in natural and artificial systems: an introductory analysis with applications to biology, control, and artificial intelligence
Propagation and storage of input information in the network with feedback
Bussei Kenkyu
Complex systems: chaos and beyond: a constructive approach with applications in life sciences
Spontaneous evolution of modularity and network motifs
Proceedings of the National Academy of Sciences of the United States of America
Chemical oscillations, waves, and turbulence
Entrainment of neuronal oscillations as a mechanism of attentional selection
Science
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