A Biophysical Basis for Molluscan Associative Learning

Abstract

The nudibranch mollusc Hermissenda crassicornis can be conditioned to change its normal positive phototactic behavior. This behavioral change is pairing specific (i.e. paired but not randomly associated light and rotation produce the change), stimulus specific, increases as a function of practice and is of long-duration (at least three to five days). The synaptic relations of identified neurons within the sensory pathways which mediate this behavior have been described in considerable detail at every stage of neural integration: sensory, interneuron, and motorneuron. With this knowledge of neural systems from input of environmental stimuli to output of animal movement, membrane changes of specific neurons were implicated as primary steps in a causal sequence responsible for the conditioning. In summary, repeated stimulus pairing results in short-term cumulative membrane depolarization (associated with elevated intracellular Ca⁺⁺) of the Type B photoreceptor. This cumulative depolarization results in long-term inactivation of an early voltage-dependent outward K⁺ current. This inactivation causes enhanced depolarizing responses of the Type B cells and, sequentially, increased inhibition of ipsilateral Type A cells, ipsilateral hair cells, interneurons and motorneurons, and ultimately retarded photo-taxis. This causal sequence is contrasted with those responsible for short-term behavioral changes such as reflex facilitation and sensitization.