Serotonin in the leech central nervous system: anatomical correlates and behavioral effects

Abstract

1. Serotonin is sequestered by a limited population of identified neurons in the 32 ganglia of the leech nervous system. A major fraction of the serotonin in each ganglion is contained in the paired Retzius cells, colossal effector neurons whose size varies longitudinally. The 5 other classes of identified serotonin-containing neurons, one effector cell and 4 interneurons, are approximately twice as numerous in anterior as in posterior ganglia. 2. We dissected 6 longitudinal samples from the ventral nerve cords of hungry Hirudo medicinalis, and measured their serotonin content using high pressure liquid chromatography with electrochemical detection. A consistent neurochemical pattern emerged in which segmental ganglia 2-4 had the highest quantity of serotonin: 18.51 pmol per ganglion. The anterior cerebral ganglion contained 14.78 pmol, and the content of the 4 posterior samples, segmental ganglia 7-10, 12-15, 17-20 and the caudal ganglion, decreased continuously from 16.35, 15.08, 10.75 to 2.51 pmol per ganglion, respectively. Morphometric analyses indicated that this pattern of ganglionic serotonin correlated primarily with longitudinal variations in the number of serotonin neurons per ganglion and secondarily with volume of the Retzius cells. Retzius cell volume correlated highly with the mass of their innervated body segments both of which are largest in mid-body domains. 3. Serotonin expresses leech feeding, and its ganglionic levels are a potentially useful index of behavioral state. We measured serotonin in the ganglionic samples from hungry and satiated leeches. The samples from recently fed animals contained 28% less serotonin than those from hungry ones. The amounts of serotonin in the cerebral and all the segmental samples from satiated leeches were significantly lower than equivalent samples of hungry animals. A similar pattern of depletion was seen in leeches which fed for a prolonged period (90 to 120 min) rather than the normal period of 30 min. 4. The effects of ingestion on serotonin-containing neurons was examined with the glyoxylic acid-induced histochemical fluorescence. The levels of fluorescence in all serotonin neurons in fed leeches were consistently lower than those in equivalent neurons in hungry animals, corroborating the ganglionic decrease in serotonin in satiated leeches. 5. To examine effects of body wall distension on serotonin levels, hungry leeches were fed to satiation, and half of them were relaxed by removing their distending blood meals. After 6 weeks, ganglionic serotonin in leeches with relaxed bodies was 21% higher than in those with distended bodies. 6. Ingestive behavior depletes serotonin from leech neurons and body wall distension appears to interfere with its synthesis.(ABSTRACT TRUNCATED AT 400 WORDS)

Applications of mRNA injections for analyzing cell lineage and asymmetric cell divisions during segmentation in the leechHelobdella robusta

“…These extra neurons arise from the nf clone (Fig. 8E,F), which could explain observations that the subesophageal ganglion contains more (N-derived) serotonergic neurons than expected from four fused standard neuromeres (Lent et al, 1991). Although we propose that it forms the anteroventral adhesive organ (Smith and Weisblat, 1994), the definitive fate of the n°clone remains to be determined.…”

Non-Associative Learning and Serotonin Induce Similar Bi-Directional Changes in Excitability of a Neuron Critical for Learning in the Medicinal Leech

“…5HT has a wide range of excitatory effects in the leech nervous system including potentiation of the swimming (Willard, 1981;O'Gara et al, 1991;Angstaadt and Friesen, 1993;Groome et al, 1993) and feeding responses (Lent et al, 1991;O'Gara et al, 1991;Groome et al, 1993) (but see Wilson et al, 1996). 5HT depolarizes the P-cell (Henderson, 1983) and facilitates recovery of conduction block in mechanosensory cells (Catarsi and Brunelli, 1991;Mar and Drapeau, 1996), which enhances their synaptic transmission onto the S-cells (Muller and Scott, 1981;Baccus et al, 2000).…”

The Activity of Isolated Neurons and the Modulatory State of an Isolated Nervous System Represent a Recent Behavioural State

“…This mechanism allows for general information to be widely spread among potential receiving cells belonging to functionally different groups and is linked to the so-called 'neuromodulatory state', which is believed to play a key role in defining functional configurations of neuronal ensembles. Changes in the content of signal molecules have been demonstrated to correlate with certain behavioural states (Glover and Lent, 1991;Lent et al, 1991;Adamo et al, 1995;Dash et al, 2009). Moreover, specific changes in extracellular neurotransmitter contents achieved by pharmacological means were reported to, at least in part, imitate a specific behavioural state (Horvitz et al, 1982;Dyakonova and Sakharov, 1995;Stevenson et al, 2005;Donnelly et al, 2013).…”