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The Journal of Neuroscience, October 19, 2005, 25(42):9807-9815; doi:10.1523/JNEUROSCI.2249-05.2005

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Behavioral/Systems/Cognitive
The Role of Sensory Network Dynamics in Generating a Motor Program

Rafael Levi,¹ Pablo Varona,^1,2 Yuri I. Arshavsky,¹ Mikhail I. Rabinovich,¹ and Allen I. Selverston¹

¹Institute for Nonlinear Science, University of California, San Diego, La Jolla, California 92093-0402, and ²Grupo de Neurocomputación Biológica, Escuela Politécnica Superior, Universidad Autónoma de Madrid, 28049 Madrid, Spain

Sensory input plays a major role in controlling motor responses during most behavioral tasks. The vestibular organs in the marine mollusk Clione, the statocysts, react to the external environment and continuously adjust the tail and wing motor neurons to keep the animal oriented vertically. However, we suggested previously that during hunting behavior, the intrinsic dynamics of the statocyst network produce a spatiotemporal pattern that may control the motor system independently of environmental cues. Once the response is triggered externally, the collective activation of the statocyst neurons produces a complex sequential signal. In the behavioral context of hunting, such network dynamics may be the main determinant of an intricate spatial behavior. Here, we show that (1) during fictive hunting, the population activity of the statocyst receptors is correlated positively with wing and tail motor output suggesting causality, (2) that fictive hunting can be evoked by electrical stimulation of the statocyst network, and (3) that removal of even a few individual statocyst receptors critically changes the fictive hunting motor pattern. These results indicate that the intrinsic dynamics of a sensory network, even without its normal cues, can organize a motor program vital for the survival of the animal.

Key words: Clione limacina; motor program; spatiotemporal pattern; hunting behavior; sensory organ; statocyst; motor coordination

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Received March 28, 2005; revised August 30, 2005; accepted September 15, 2005.

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