Associative memory in three aplysiids: Correlation with heterosynaptic modulation

Abstract

Much recent research on mechanisms of learning and memory focuses on the role of heterosynaptic neuromodulatory signaling. Such neuromodulation appears to stabilize Hebbian synaptic changes underlying associative learning, thereby extending memory. Previous comparisons of three related sea-hares (Mollusca, Opisthobranchia) uncovered interspecific variation in neuromodulatory signaling: strong in Aplysia californica, immeasureable in Dolabrifera dolabrifera, and intermediate in Phyllaplysia taylori. The present study addressed whether this interspecific variation in neuromodulation is correlated with memory of associative (classical conditioning) learning. We differentially conditioned the tail-mantle withdrawal reflex of each of the three species: Mild touch to one side of the tail was paired with a noxious electrical stimulus to the neck. Mild touch to the other side served as an internal control. Post-training reflex amplitudes were tested 15-30 min after training and compared with pre-test amplitudes. All three species showed conditioning: training increased the paired reflex more than the unpaired reflex. However, the temporal pattern of conditioning varied between species. Aplysia showed modest conditioning that grew across the post-test period. Dolabrifera showed distinctly short-lived conditioning, present only on the first post-test. The time course of memory in Phyllaplysia was intermediate, although not statistically distinguishable from the other two species. Taken together, these experiments suggest that evolutionary changes in nonassociative heterosynaptic modulation may contribute to evolutionary changes in the stability of the memory of classical conditioning.Contemporary models of learning and memory (Frey et al. 1990(Frey et al. , 2001 Bailey et al. 2000a,b;Almaguer-Meliana et al. 2005) propose that heterosynaptic modulation during a learning event serves to stabilize Hebbian mechanisms of synaptic plasticity, thereby increasing the persistence of associative neural changes underlying several forms of learning and memory, including classical (Pavlovian) conditioning. This model suggests an evolutionary hypothesis: that evolutionary change in nonassociative heterosynaptic modulation should be associated with a concomitant change in the duration of associative memory.A test of this hypothesis is afforded by the recent discovery of interspecific variation in nonassociative behavioral sensitization, and the heterosynaptic modulation that underlies it, in opisthobranch relatives of the model species, Aplysia californica. Modulation is produced by application of the modulatory transmitter, serotonin (Wright et al. 1996;Erixon et al. 1999), or by strong stimulation of peripheral nerves . Both of these nonassociative manipulations cause neuromodulatory changes in sensory-neuron firing properties of Aplysia, but their effects on two related species are much weaker. Specifically, in Dolabrifera dolabrifera, no serotonin-induced changes are observed, and a cladistic analysis (Wright et al. 1996) strongly s...

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“…Similarly, researchers may ask whether a species difference in some behavioral trait or cognitive capacity correlates with specific molecular, neuroanatomical, or neurophysiological features. Such a comparative approach revealed, for example, that species differences in associative learning among three species of sea hares, including the well-known Aplysia californica , correlate well with differences in neuromodulation [Hoover et al, 2006]. This comparative finding helps to link experimental studies in Aplysia to general proposals about the mechanisms underlying learning and memory.…”