Chaos in the Brain

Henri Korn*, Philippe Faure

The search for chaotic patterns has occupied numerous investigators in neuroscience, as in many other fields of science. Their results and main conclusions are reviewed in the light of the most recent criteria that need to be satisfied since the first descriptions of the surrogate strategy. The methods used in each of these studies have almost invariably combined the analysis of experimental data with simulations using formal models, often based on modified Huxley and Hodgkin equations and/or of the Hindmarsh and Rose models of bursting neurons. Due to technical limitations, the results of these simulations have prevailed over experimental ones in studies on the nonlinear properties of large cortical networks and higher brain functions. Yet, and although a convincing proof of chaos (as defined mathematically) has only been obtained at the level of axons, of single and coupled cells, convergent results can be interpreted as compatible with the notion that signals in the brain are distributed according to chaotic patterns at all levels of its various forms of hierarchy.

This chronological account of the main landmarks of nonlinear neurosciences follows an earlier publication [Faure, Korn, C. R. Acad. Sci. Paris, Ser. III 324 (2001) 773–793] that was focused on the basic concepts of nonlinear dynamics and methods of investigations which allow chaotic processes to be distinguished from stochastic ones and on the rationale for envisioning their control using external perturbations. Here we present the data and main arguments that support the existence of chaos at all levels from the simplest to the most complex forms of organization of the nervous system.

We first provide a short mathematical description of the models of excitable cells and of the different modes of firing of bursting neurons (Section 1). The deterministic behavior reported in giant axons (principally squid), in pacemaker cells, in isolated or in paired neurons of Invertebrates acting as coupled oscillators is then described (Section 2). We also consider chaotic processes exhibited by coupled Vertebrate neurons and of several components of Central Pattern Generators (Section 3). It is then shown that as indicated by studies of synaptic noise, deterministic patterns of firing in presynaptic interneurons are reliably transmitted, to their postsynaptic targets, via probabilistic synapses (Section 4).

This raises the more general issue of chaos as a possible neuronal code and of the emerging concept of stochastic resonance Considerations on cortical dynamics and of EEGs are divided in two parts. The first concerns the early attempts by several pioneer authors to demonstrate chaos in experimental material such as the olfactory system or in human recordings during various forms of epilepsies, and the belief in ‘dynamical diseases’ (Section 5). The second part explores the more recent period during which surrogate-testing, definition of unstable periodic orbits and period-doubling bifurcations have been used to establish more firmly the nonlinear features of retinal and cortical activities and to define predictors of epileptic seizures (Section 6).

Finally studies of multidimensional systems have founded radical hypothesis on the role of neuronal attractors in information processing, perception and memory and two elaborate models of the internal states of the brain (i.e. ‘winnerless competition’ and ‘chaotic itinerancy’). Their modifications during cognitive functions are given special attention due to their functional and adaptive capabilities (Section 7) and despite the difficulties that still exist in the practical use of topological profiles in a state space to identify the physical underlying correlates. The reality of ‘neurochaos’ and its relations with information theory are discussed in the conclusion (Section 8) where are also emphasized the similarities between the theory of chaos and that of dynamical systems. Both theories strongly challenge computationalism and suggest that new models are needed to describe how the external world is represented in the brain. To cite this article: H. Korn, P. Faure, C. R. Biologies 326 (2003).

2003 Académie des sciences. Published by Elsevier SAS. All rights reserved.

Keywords: neuronal dynamics; neurochaos; networks; chaotic itinerancy; winnerless competition; representation; neuronal code