Plasticity in a cerebellar-like structure: Suppressing reafference during episodic behaviors

Detection of relevant sensory signals requires the filtering out of irrelevant noise, including noise created by the animal's own movements (reafference). This is accomplished in the electrosense of little skates (Raja erinacea) by an adaptive filter in the cerebellar-like electrosensory nucleus (dorsal nucleus) in the medulla. We have shown that electrosensory inputs reliably coupled to the regularly recurring movements of breathing over time are eliminated selectively in the principal neurons (ascending efferent neurons, AENs) by a cancellation signal that is a negative of the reafference and is supplied by a parallel fiber system. Similarly, electrosensory inputs repeatedly linked to passive fin movements are eliminated suggesting that the filter also functions in relation to other behaviors besides breathing. To determine whether this adaptive filter can eliminate reafference created by brief and infrequent episodic behaviors like swimming in skates, we initiated a series of coupling tests in which an external electrosensory stimulus was coupled to short bouts of either parallel fiber stimulation or passive fin movements, and then measured the ability of AENs to generate a cancellation signal. Following five brief coupling periods (30-60 s) separated by long rest periods (1-9 min), 38.5% of the AENs developed a cancellation signal when the coupling was to parallel fiber stimulation, and 73% when the coupling was to passive fin movement. We demonstrate that the cancellation signals can be developed incrementally, persist for at least a 3 h rest period without reinforcement, and are extinguished within minutes when the association of sensory stimulus and fin movement or parallel fiber stimulation no longer exists. The results indicate that the adaptive filter has the properties necessary to cancel reafference associated with even brief and infrequent behaviors.