Serotonergic cerebral cells control activity of cilia in the foregut of the pteropod mollusk Clione limacina

Abstract

Bilaterally symmetrical pair of serotonergic cells, named C1 in Clione, has been described in the cerebral ganglia of all gastropod species. Here we describe a new role of C1 cells in gastropod mollusks: control of activity of ciliated epithelium in the foregut. Detailed morphological investigation of C1 neurons in the pteropod mollusk Clione limacina revealed that these cells among other destinations send their neurites into foregut where they produce intense arborization with large varicosities along the processes. Intracellular stimulation of a single C1 induced pronounced activation (often followed by inhibition) of cilia lining the foregut. This activation was substantially reduced by serotonin antagonist mianserin. Bath application of serotonin also induced transient increase in ciliary transport rate, followed by inhibition of ciliary activity up to its full cessation in some areas of isolated foregut. These data suggest that C1 in Clione may use serotonin to influence cilia in the foregut. Taking into account high homology of serotonergic cerebral cells across studied species we can speculate that these cells may be involved in the neural control of cilia in the foregut in other gastropod mollusks.

The distribution and evolutionary dynamics of dopaminergic neurons in molluscs

“…Both Clione and Melibe are recognized reference species in evolutionary neurobiology, with the identification of multiple neurons controlling feeding, swimming, and other behaviors (Sakharov, 1970; Gerasimov, 1973; Sakharov, 1974; Arshavsky Yu et al, 1985; Satterlie, 1985; Arshavsky Yu et al, 1989; Norekian, 1990a; Kabotyanskii and Sakharov, 1991; Page, 1992b; a; Satterlie, 1993; Norekian and Satterlie, 1996; Arshavsky et al, 1998; Deliagina et al, 1998; Moroz et al, 2000; Sadreyev and Panchin, 2000; Newcomb and Watson, 2001; 2002; Thompson and Watson, 2005; Kempf, 2008; Malyshev and Balaban, 2011; Satterlie, 2013; Duback et al, 2018; Sakurai and Katz, 2019; Pirtle, 2022). Nonetheless, very little is known about dopaminergic signaling (Sakharov and Kabotyanski, 1986; Kabotyanski and Sakharov, 1988; Norekian, 1990b) in these ecologically important groups, and the initial mapping of catecholaminergic neurons in Clione was performed using modified aldehyde-induced fluorescence techniques (Kabotyanski and Sakharov, 1989).…”