Behavioral and neural bases of noncoincidence learning in Hermissenda

Neurobiological studies of associative learning and memory have focused nearly exclusively on the analysis of neural plasticity resulting from paired stimuli. A second major category of associative-learning processes, one that has been conspicuously neglected in cellular studies, is that of conditioned inhibition (CI), learning that one stimulus signals the absence of another. The physiological bases of CI are obscure and unexplored. To study the behavioral and neural bases of CI, we exposed the nudibranch mollusc Hermissenda crassicornis to explicitly unpaired (EU) presentations of light and rotation. We report here that Hermissenda exhibited persistent increases in phototactic behavior after EU training. Retardation-of-learning test results provided further evidence that EU animals learned that light signaled the absence of rotation. The increased phototactic behavior of EU animals was paralleled by selective decreases in the magnitude of ocular type B cell photoresponses and the frequency of light-elicited action potentials: the first report of a neural correlate of noncoincidence learning. Plasticity arising from explicitly unpaired stimulus presentations raises provocative questions as to how noncoincidence is detected and represented within the nervous system.