The long-term resetting of a brainstem pacemaker nucleus by synaptic input: a model for sensorimotor adaptation.

The cellular mechanisms behind sensorimotor adaptations, such as the adaptation to a sustained change in visual inputs by prism goggles in humans, are not known. Here we present a novel example of long-term sensorimotor adaptation in a well known neuroethological model, the jamming-avoidance response of a weakly electric fish. The adaptation is relatively long lasting, up to 9 hr in vivo, and is likely to be mediated by NMDA receptors. We demonstrate in a brain slice preparation that the pacemaker nucleus is the locus of adaptation and that it responds to long-lasting synaptic stimulation with an increase in the postsynaptic spike frequency persisting for hours after stimulus termination. The mechanism for the neuronal memory behaves as an integrator, and memory duration and strength are quantitatively related to the estimated amount of synaptic stimulation. This finding is contrary to the idea that neurons respond solely to long-lasting synaptic input by turning down their intrinsic excitability. We show that this positive feedback at the cellular level actually contributes to a negative feedback loop at the organismic level if the entire neural circuit and the behavioral link are considered.