Evolutionary origins and principles of distributed neural computation for state estimation and movement control in vertebrates

Department of Zoology and Centre for Neuroscience, University of Otago, Dunedin, New ZealandReceived October 22, 2004; revised December 2, 2004; accepted December 10, 2004Vertebrates are mostly large, agile creatures that can move rapidly and efficiently despite the significant inertialand interaction forces that are generated when they move. Vertebrates appear in the fossil record in the lowerCambrian, when predation began to apply selection pressure for increased size and, consequently, increasedinertia. Agility depends critically upon the cerebellum, a brain structure that appears to have evolved as anelaboration of the vestibular and lateral-line sensory processing regions in brains of aquatic ancestors. There iscompelling evidence to suggest that the specific role of the cerebellum in motor control (etc) is state estimation.Analysis of responses of vestibular neurons in bullfrogs shows that these neurons have fractional-order dynam-ics. Because of this property, the vestibular nerve forms a map of the state space of the animal’s head, andindividual action potentials can be regarded as assertions about the location of the head in that space. This viewof vestibular coding suggests an analogy with particle filters, a new simulation-based method for stateestimation. In a particle filter the distribution of possible states consistent with observations is represented by acloud of “particles” in a map of the state space. By regarding action potentials as particles in neural stateestimators, we may develop a realistic model of neural computation in the cerebellum. At the same time—andindependently of the biological verisimilitude of such a cerebellar model—we may develop useful new algo-rithms for state estimation. © 2005 Wiley Periodicals, Inc. Complexity 10: , 2005