PHYLOGENETIC ANALYSIS OF LEARNING‐RELATED NEUROMODULATION IN MOLLUSCAN MECHANOSENSORY NEURONS

Autor: Barbara J. Maynard, William G. Wright, Daniel E. Rozen, David Kirschman
Rok vydání: 1996
Předmět:
Zdroj: Scopus-Elsevier
ISSN: 1558-5646
0014-3820
DOI: 10.1111/j.1558-5646.1996.tb03614.x
Popis: In spite of significant advances in our understanding of mechanisms of learning and memory in a variety of organisms, little is known about how such mechanisms evolve. Even mechanisms of simple forms of learning, such as habituation and sensitization, have not been studied phylogenetically. Here we begin an evolutionary analysis of learning-related neuromodulation in species related to the well-studied opisthobranch gastropod, Aplysia californica. In Aplysia, increased spike duration and excitability in mechanosensory neurons contribute to several forms of learning-related changes to defensive withdrawal reflexes. The modulatory transmitter serotonin (5-hydroxytryptamine, or 5-HT), is thought to play a critical role in producing these firing property changes. In the present study, we tested mechanosensory homologs of the tail-withdrawal reflex in species related to Aplysia for 5-HT-mediated increases in spike duration and excitability. Criteria used to identify homologous tail-sensory neurons included position, relative size, resting electrical properties, expression of a sensory neuron-specific protein, neuroanatomy, and receptive field. The four ingroup species studied (Aplysia californica, Dolabella auricularia, Bursatella leachii, and Dolabrifera dolabrifera) belong to two clades (two species each) within the family Aplysiidae. In the first clade (Aplysia/Dolabella), we found that the tail-sensory neurons of A. californica and tail-sensory homologs of a closely related species, D. auricularia, responded to bath-applied serotonin in essentially similar fashion: significant increases in spike duration as well as excitability. In the other clade (Dolabrifera/Bursatella), more distantly related to Aplysia, one species (B. leachii) showed spike broadening and increased excitability. However, the other species (D. dolabrifera) showed neither spike broadening nor increased excitability. The firing properties of tail-sensory homologs of D. dolabrifera were insensitive to 5-HT over a wide range of concentrations. We also performed experiments on two outgroup species (Akera bullata and Bulla gouldiana) and found that spike duration was unaffected by 5-HT, whereas excitability was increased. This study suggests that 5-HT-induced spike broadening arose more recently in opisthobranch evolution, whereas 5-HT-induced excitability increase is a more ancestral trait that may have been expressed in the earliest opisthobranchs. Both traits are absent in the aplysiid species D. dolabrifera, demonstrating that a lineage can lose learning-related mechanisms. The phylogenetic variation observed in the present study presents the opportunity to test general models about learning mechanisms and their evolution in unique ways.
Databáze: OpenAIRE
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