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The Journal of Neuroscience, February 13, 2008, 28(7):1598-1612; doi:10.1523/JNEUROSCI.4946-07.2008

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Behavioral/Systems/Cognitive
Transformations of Electrosensory Encoding Associated with an Adaptive Filter

Nathaniel B. Sawtell and Alan Williams

Neurological Sciences Institute, Oregon Health & Sciences University, Beaverton, Oregon 97006

Correspondence should be addressed to Nathaniel B. Sawtell, Neurological Sciences Institute, Oregon Health & Sciences University, Beaverton, OR 97006. Email: sawtelln{at}ohsu.edu

Sensory information is often acquired through active exploration. However, an animal's own movements may result in changes in patterns of sensory input that could interfere with the detection and processing of behaviorally relevant sensory signals. Neural mechanisms for predicting the sensory consequences of movements are thus likely to be of general importance for sensory systems. Such mechanisms have been identified in cerebellum-like structures associated with electrosensory processing in fish. These structures are hypothesized to act as adaptive filters, removing correlations between incoming sensory input and central predictive signals through associative plasticity at parallel fiber synapses. The present study tests the adaptive filter hypothesis in the electrosensory lobe (ELL) of weakly electric mormyrid fish. We compared the ability of electroreceptors and ELL efferent neurons to encode the position of moving objects in the presence and absence of self-generated electrosensory signals caused by tail movements. Tail movements had strong effects on the responses of electroreceptors, substantially reducing the amount of information they conveyed about object position. In contrast, responses of efferent neurons were relatively unaffected by tail movements, and the information they conveyed about object position was preserved. We provide evidence that the electrosensory consequences of tail bending are opposed by proprioceptive inputs conveyed by parallel fibers and that the effects of proprioceptive inputs to efferent cells are plastic. These results support the idea that cerebellum-like structures learn and remove the predictable sensory consequences of behavior and link mechanisms of adaptive filtering to selective encoding of behaviorally relevant sensory information.

Key words: synaptic plasticity; cerebellum; electrosensory; neuroethology; proprioception; corollary discharge

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Received Nov. 2, 2007; revised Dec. 14, 2007; accepted Jan. 4, 2008.

Correspondence should be addressed to Nathaniel B. Sawtell, Neurological Sciences Institute, Oregon Health & Sciences University, Beaverton, OR 97006. Email: sawtelln{at}ohsu.edu

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