title: Identification and evolutionary implications of neurotransmitter-ciliary interactions underlying the behavioral response to hypoxia in Lymnaea stagnalis embryos.
abstract: Acceleration of embryonic rotation is a common response to hypoxia among pond snails. It was first characterized in Helisoma trivolvis embryos, which have a pair of sensorimotor neurons that detect hypoxia and release serotonin onto postsynaptic ciliary cells. The objective of the present study was to determine how the hypoxia response is mediated in Lymnaea stagnalis, which differ from H. trivolvis by having both serotonergic and dopaminergic neurons, and morphologically distinct ciliated structures at comparative stages of embryonic development. Time-lapse video recordings of the rotational behavior in L. stagnalis revealed similar rotational features to those previously observed in H. trivolvis, including rotational surges and rotational responses to hypoxia. Serotonin and dopamine increased the rate of rotation with similar potency. In contrast, serotonin was more potent than dopamine in stimulating the ciliary beat frequency of isolated pedal cilia. Isolated apical plate cilia displayed an irregular pattern of ciliary beating that precluded the measurement of ciliary beat frequency. A qualitative assessment of ciliary beating revealed that both serotonin and dopamine were able to stimulate apical plate cilia. The ciliary responses to dopamine were reversible in both pedal and apical plate cilia, whereas the responses to serotonin were only reversible at concentrations below 100 μmol l(-1). Mianserin, a serotonin receptor antagonist, and SKF83566, a dopamine receptor antagonist, effectively blocked the rotational responses to serotonin and dopamine, respectively. The rotational response to hypoxia was only partially blocked by mianserin, but was fully blocked by SKF83566. These data suggest that, despite the ability of serotonin to stimulate ciliary beating in L. stagnalis embryos, the rotational response to hypoxia is primarily mediated by the transient apical catecholaminergic neurons that innervate the ciliated apical plate.
authors.affiliation: Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada. jeff.goldberg@ucalgary.ca
authors.forename: Jeffrey I
authors.initials: JI
authors.lastname: Goldberg
authors.forename: Darren R
authors.initials: DR
authors.lastname: Rich
authors.forename: Siva P
authors.initials: SP
authors.lastname: Muruganathan
authors.forename: Maple B
authors.initials: MB
authors.lastname: Liu
authors.forename: Julia R
authors.initials: JR
authors.lastname: Pon
authors.forename: Rose
authors.initials: R
authors.lastname: Tam
authors.forename: Thomas J
authors.initials: TJ
authors.lastname: Diefenbach
authors.forename: Shihuan
authors.initials: S
authors.lastname: Kuang
mesh_terms: D015647:2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine / Q000031:analogs & derivatives / Q000494:pharmacology; D000693:Anaerobiosis / Q000187:drug effects; D000818:Animals; D001522:Behavior, Animal / Q000187:drug effects; D005075:Biological Evolution; D002923:Cilia / Q000187:drug effects / Q000378:metabolism*; D004298:Dopamine / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000187:drug effects / Q000378:metabolism*; D005455:Fluorescent Antibody Technique; D008195:Lymnaea / Q000187:drug effects / Q000196:embryology* / Q000378:metabolism*; D008803:Mianserin / Q000494:pharmacology; D018377:Neurotransmitter Agents / Q000378:metabolism*; D012399:Rotation; D012701:Serotonin / Q000378:metabolism; D013997:Time Factors
chemical_list: D015647:2,3,4,5-Tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine; D004298:Dopamine; D008803:Mianserin; D018377:Neurotransmitter Agents; D012701:Serotonin; C044846:SKF83566