Distributed Dynamical Computation in Neural Circuits with Propagating Coherent Activity Patterns

Activity in neural circuits is spatiotemporally organized. Its spatial organization consists of multiple, localized coherent patterns, or patchy clusters. These patterns propagate across the circuits over time. This type of collective behavior has ubiquitously been observed, both in spontaneous activity and evoked responses; its function, however, has remained unclear. We construct a spatially extended, spiking neural circuit that generates emergent spatiotemporal activity patterns, thereby capturing some of the complexities of the patterns observed empirically. We elucidate what kind of fundamental function these patterns can serve by showing how they process information. As self-sustained objects, localized coherent patterns can signal information by propagating across the neural circuit. Computational operations occur when these emergent patterns interact, or collide with each other. The ongoing behaviors of these patterns naturally embody both distributed, parallel computation and cascaded logical operations. Such distributed computations enable the system to work in an inherently flexible and efficient way. Our work leads us to propose that propagating coherent activity patterns are the underlying primitives with which neural circuits carry out distributed dynamical computation.Author Summary: The brain processes information with extraordinary efficiency, and can perform feats such as effortlessly recognizing objects from among thousands of possibilities within a fraction of a second. This is accomplished because the brain represents and processes information in a distributed fashion and in a dynamical way. This processing is manifested in spatiotemporal neural activity patterns of great complexities within the brain. Here, we construct a spiking neural circuit that can reproduce some of the complexities, which are evident in terms of multiple wave patterns with interactions between each other. We show that their dynamics can support propagating pattern-based computation; spiking wave patterns signal information by propagating across neural circuits, and computational operations occur when they collide with each other. Such dynamical computation contrasts sharply with that done by static and physically fixed logic gates operating in other computing machines such as computers. Moreover, we elucidate that the collective dynamics of multiple, interacting wave patterns enable computation processing implemented in a fundamentally distributed and parallel manner in the neural circuit.