Evolution of Learning in Three Aplysiid Species: Differences in Heterosynaptic Plasticity Contrast with Conservation in Serotonergic Pathways

Marinesco, Stéphane; Duran, Kristy L.; Wright, William G.

doi:10.1113/jphysiol.2003.038356

Cited by 19 publications

(13 citation statements)

References 47 publications

(180 reference statements)

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“…Thus, the evidence for intermediate memory is relatively weak. Nevertheless, if the memory is indeed intermediate, it is consistent with the intermediate level of serotonin signaling and sensitization observed in Phyllaplysia (Erixon et al 1999;Marinesco et al 2003).…”

Section: Discussionsupporting

confidence: 50%

“…Consistent with this loss, strong stimulation of peripheral nerves in Dolabrifera induces no change in sensory neuron firing properties . In contrast, such stimulation causes robust changes to sensoryneuron firing properties in Aplysia (Walters et al 1983;Marinesco et al 2003). These neurobiological differences in modulatory phenotype extend to the behavioral level as well: Dolabrifera shows no evidence of dishabituation or short-or long-term sensitization following noxious stimuli, which routinely causes both forms of learning in Aplysia (Wright 1998).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, in a wide variety of systems, heterosynaptic modulation appears to "stabilize" synaptic changes induced by associative (Hebbian) protocols. A reasonable extension of these models predicts that the evolutionary loss of modulation by serotonin in Dolabrifera (Wright 1998), and the relatively lower level of modulation caused by noxious stimuli in Phyllaplysia , should limit the stability of associative memory in these species relative to Aplysia, whose heterosynaptic modulation and behavioral sensitization in response to noxious stimuli is robust (e.g., Walters et al 1983;Wright 1998;Marinesco et al 2003;Bristol et al 2004; for review, see Barbas et al 2003). The results of the present study are consistent with that prediction, thereby strengthening the idea that evolutionary Phylogenetic correlation between memory and modulation…”

Section: Discussionmentioning

confidence: 99%

“…We decided to test for classical conditioning in a third aplysiid, Phyllaplysia taylori, which was previously observed to have limited heterosynaptic modulation in response to nerve shock and only localized sensitization in response to noxious stimuli (Erixon et al 1999;Marinesco et al 2003). This species was thus expected to show intermediate duration of memory for classical conditioning.…”

Section: Learning and Memory 821mentioning

confidence: 99%

“…www.learnmem.org strong evidence of both, and Dolabrifera showing no evidence of either (Wright et al 1996;Wright 1998;Marinesco et al 2003). We decided to test for classical conditioning in a third aplysiid, Phyllaplysia taylori, which was previously observed to have limited heterosynaptic modulation in response to nerve shock and only localized sensitization in response to noxious stimuli (Erixon et al 1999;Marinesco et al 2003).…”

Section: Learning and Memory 821mentioning

confidence: 99%

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Associative memory in three aplysiids: Correlation with heterosynaptic modulation

Hoover¹,

Nguyen²,

Thompson³

et al. 2006

Learn. Mem.

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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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Section: Discussionsupporting

confidence: 50%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Learning and Memory 821mentioning

confidence: 99%

Section: Learning and Memory 821mentioning

confidence: 99%

See 3 more Smart Citations

Associative memory in three aplysiids: Correlation with heterosynaptic modulation

Hoover¹,

Nguyen²,

Thompson³

et al. 2006

Learn. Mem.

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Evolution of Motor Systems

Katz

Hale

2017

Neurobiology of Motor Control

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Comparative mapping of serotonin‐immunoreactive neurons in the central nervous systems of nudibranch molluscs

Newcomb

Fickbohm

Katz

2006

J of Comparative Neurology

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The serotonergic systems in nudibranch molluscs were compared by mapping the locations of serotonin-immunoreactive (5-HT-ir) neurons in 11 species representing all four suborders of the nudibranch clade: Dendronotoidea (Tritonia diomedea, Tochuina tetraquetra, Dendronotus iris, Dendronotus frondosus, and Melibe leonina), Aeolidoidea (Hermissenda crassicornis and Flabellina trophina), Arminoidea (Dirona albolineata, Janolus fuscus, and Armina californica), and Doridoidea (Triopha catalinae). A nomenclature is proposed to standardize reports of cell location in species with differing brain morphologies. Certain patterns of 5-HT immunoreactivity were found to be consistent for all species, such as the presence of 5-HT-ir neurons in the pedal and cerebral ganglia. Also, particular clusters of 5-HT-ir neurons in the anterior and posterior regions of the dorsal surface of the cerebral ganglion were always present. However, there were interspecies differences in the number of 5-HT-ir neurons in each cluster, and some clusters even exhibited strong intraspecies variability that was only weakly correlated with brain size. Phylogenetic analysis suggests that the presence of particular classes of 5-HT-ir neurons exhibits a great deal of homoplasy. The conserved features of the nudibranch serotonergic system presumably represent the shared ancestral structure, whereas the derived characters suggest substantial independent evolutionary changes in the number and presence of serotonergic neurons. Although a number of studies have demonstrated phylogenetic variability of peptidergic systems, this study suggests that serotonergic systems may also exhibit a high degree of homoplasy in some groups of organisms.

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Evolution of Learning in Three Aplysiid Species: Differences in Heterosynaptic Plasticity Contrast with Conservation in Serotonergic Pathways

Cited by 19 publications

References 47 publications

Associative memory in three aplysiids: Correlation with heterosynaptic modulation

Associative memory in three aplysiids: Correlation with heterosynaptic modulation

Evolution of Motor Systems

Comparative mapping of serotonin‐immunoreactive neurons in the central nervous systems of nudibranch molluscs

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