Pedal serotonergic neuron clusters of the pteropod mollusc, Clione limacina , contain two morphological subtypes with di

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ORIGINAL ARTICLE

Pedal serotonergic neuron clusters of the pteropod mollusc, Clione limacina, contain two morphological subtypes with different innervation targets Jennifer B. Plyler1 · Richard A. Satterlie1  Received: 6 February 2020 / Accepted: 31 October 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Each pedal ganglion of the pteropod mollusc Clione limacina contains a cluster of serotonin-immunoreactive neurons that have been shown to modulate contractions of the slow-twitch musculature of the wing-like parapodia, and contribute to swim accelerations. Each cluster has a variable number of neurons, between 5 and 9, but there is no significant difference between right and left ganglia. In experiments with electrophysiological recordings followed by dye-injection (carboxyfluorescein), the clusters were found to contain two subsets of neurons. The majority innervate the ipsilateral wing via nerve n4. Two of the neurons in each cluster send processes out of the pedal ganglion in nerves n3 and n8. The processes in nerve n3 innervate the body wall of the neck region, while those in nerve n8 innervate the body wall of the tail. The baseline electrophysiological activity of the two subsets of neurons was different as “wing” neurons had constant barrages of small synaptic activity, while the “body wall” neurons had few synaptic inputs. The potential roles of the Pd-SW cluster in swim acceleration (wing neurons) and control of fluid pressure in the body and wing hemocoelic compartments (body wall neurons) are discussed. Keywords  Mollusc · Swimming · Serotonin · Pteropod · Neuron morphology

Introduction Changes in locomotory speed typically involve increases in the frequency of movement of locomotory structures as well as increases in the force or amplitude of the movements. The neuronal basis of locomotory accelerations has been studied in detail in zebra fish, where interneurons are recruited into the central control circuitry in a predictable manner relative to locomotory speed (McLean et al. 2008; McLean and Fetcho 2009; Ausborn et al. 2012; Eklof-Ljunggren et al. 2012; Ampatzis et al. 2014; Bjornfors et al. 2019; Song et al. 2020). Similar results have been found in mice (Dougherty and Kiehn 2010; Zhong et al. 2010, 2011; Bjornfors et al. 2019). At the physiological level, motorneuron recruitment also follows a predictable order (Gabriel et al. 2011) that is matched with the recruitment of interneuron modules * Richard A. Satterlie [email protected] 1



Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC 28409, USA

(Ausborn et al. 2012; Ampatzis et al. 2014; Bjornfors et al. 2019). The pteropod mollusk, Clione limacina, shows two distinct swimming speeds, and the change from slow to fast swimming is equivalent to a gait change in vertebrates (Arshavsky et al. 1985a,b,c,d; Satterlie and Norekian 1997, 2001). The locomotory appendages of Clione consist of foot tissue that is laterally expanded into a pair of winglike parapodia (called wi