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Appropriate generalization of learned responses to new situations is vital for adaptive behavior. We provide a circuit-level account of generalization in the electrosensory lobe (ELL) of weakly electric mormyrid fish. Much is already known in this system about a form of learning in which motor corollary discharge signals cancel responses to the uninformative input evoked by the fish’s own electric pulses. However, for this cancellation to be useful under natural circumstances, it must generalize accurately across behavioral regimes, specifically different electric pulse rates. We show that such generalization indeed occurs in ELL neurons, and develop a circuit-level model explaining how this may be achieved. The mechanism involves regularized synaptic plasticity and an approximate matching of the temporal dynamics of motor corollary discharge and electrosensory inputs. Recordings of motor corollary discharge signals in mossy fibers and granule cells provide direct evidence for such matching.