Evolution of nonassociative learning: behavioral analysis of a phylogenetic lesion.

A recent phylogenetic analysis of two learning-related neuromodulatory traits in mechanosensory neurons of species related to the marine mollusk Aplysia californica identified one species, Dolabrifera dolabrifera, which lacked both neuromodulatory traits. Since these traits are thought to contribute importantly to certain forms of learning and memory in the defensive withdrawal reflexes of Aplysia, in the present study, I tested the prediction that facilitatory nonassociative learning would be reduced or absent in Dolabrifera. I tested the tail-mantle withdrawal reflex in Dolabrifera and size-matched Aplysia for three forms of nonassociative learning and memory: dishabituation and short- and long-term sensitization. I found that the same protocols that produced significant dishabituation, short-term sensitization, and long-term sensitization in Aplysia failed in all three cases to produce significant learning in Dolabrifera. Thus, the prediction from the prior mechanistic analysis is confirmed: Dishabituation and short- and long-term sensitization are significantly reduced and perhaps abolished in Dolabrifera. Although not conclusive, this phylogenetic correlation between the absence of behavioral changes and the absence of neural mechanisms thought to underlie the behavioral changes gives support to the contemporary neuromodulatory model of dishabituation and sensitization in Aplysia. Furthermore, these results raise the possibility that evolutionary alteration of two specific neuromodulatory mechanisms may have directly contributed to evolutionary change in behavioral plasticity.