Spatial-specific action of serotonin within the leech midbody ganglion

Calviño, María Ana; Szczupak, Lidia

doi:10.1007/s00359-008-0326-2

Cited by 12 publications

(10 citation statements)

References 48 publications

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“…To elevate serotonin levels, we used the selective serotonin re-uptake inhibitor, fluoxetine ( Figure 5C ). Unlike the exogenous application of 5-HT, fluoxetine should specifically concentrate serotonin at naturally occurring release sites ( Calviño and Szczupak, 2008 ; Calviño et al, 2005 ). Consistent with an inhibitory function for serotonin, fluoxetine decreased DA1 PN odor responses ( Figure 6D ).…”

Section: Resultsmentioning

confidence: 99%

Functional integration of a serotonergic neuron in the Drosophila antennal lobe

Zhang

Gaudry

2016

eLife

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Serotonin plays a critical role in regulating many behaviors that rely on olfaction and recently there has been great effort in determining how this molecule functions in vivo. However, it remains unknown how serotonergic neurons that innervate the first olfactory relay respond to odor stimulation and how they integrate synaptically into local circuits. We examined the sole pair of serotonergic neurons that innervates the Drosophila antennal lobe (the first olfactory relay) to characterize their physiology, connectivity, and contribution to pheromone processing. We report that nearly all odors inhibit these cells, likely through connections made reciprocally within the antennal lobe. Pharmacological and immunohistochemical analyses reveal that these neurons likely release acetylcholine in addition to serotonin and that exogenous and endogenous serotonin have opposing effects on olfactory responses. Finally, we show that activation of the entire serotonergic network, as opposed to only activation of those fibers innervating the antennal lobe, may be required for persistent serotonergic modulation of pheromone responses in the antennal lobe.DOI: http://dx.doi.org/10.7554/eLife.16836.001

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Section: Resultsmentioning

confidence: 99%

Functional integration of a serotonergic neuron in the Drosophila antennal lobe

Zhang

Gaudry

2016

eLife

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“…An equivalent amount of serotonin is secreted by the other Retzius neuron in the ganglion, since both respond in parallel upon the activation of common synaptic inputs (Velázquez-Ulloa et al, 2003). Therefore it is not surprising that a neuron pair is capable of producing the multiple modulatory effects of serotonin seen in the leech (Willard, 1981; Kristan and Nusbaum, 1982; Burrell et al, 2002; Crisp and Mesce, 2006; Calviño and Szczupak, 2008; Bisson and Torre, 2011). …”

Section: Discussionmentioning

confidence: 99%

Cycling of Dense Core Vesicles Involved in Somatic Exocytosis of Serotonin by Leech Neurons

Trueta¹,

Kuffler²,

De‐Miguel³

2012

Front. Physio.

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We studied the cycling of dense core vesicles producing somatic exocytosis of serotonin. Our experiments were made using electron microscopy and vesicle staining with fluorescent dye FM1-43 in Retzius neurons of the leech, which secrete serotonin from clusters of dense core vesicles in a frequency-dependent manner. Electron micrographs of neurons at rest or after 1 Hz stimulation showed two pools of dense core vesicles. A perinuclear pool near Golgi apparatuses, from which vesicles apparently form, and a peripheral pool with vesicle clusters at a distance from the plasma membrane. By contrast, after 20 Hz electrical stimulation 47% of the vesicle clusters were apposed to the plasma membrane, with some omega exocytosis structures. Dense core and small clear vesicles apparently originating from endocytosis were incorporated in multivesicular bodies. In another series of experiments, neurons were stimulated at 20 Hz while bathed in a solution containing peroxidase. Electron micrographs of these neurons contained gold particles coupled to anti-peroxidase antibodies in dense core vesicles and multivesicular bodies located near the plasma membrane. Cultured neurons depolarized with high potassium in the presence of FM1-43 displayed superficial fluorescent spots, each reflecting a vesicle cluster. A partial bleaching of the spots followed by another depolarization in the presence of FM1-43 produced restaining of some spots, other spots disappeared, some remained without restaining and new spots were formed. Several hours after electrical stimulation the FM1-43 spots accumulated at the center of the somata. This correlated with electron micrographs of multivesicular bodies releasing their contents near Golgi apparatuses. Our results suggest that dense core vesicle cycling related to somatic serotonin release involves two steps: the production of clear vesicles and multivesicular bodies after exocytosis, and the formation of new dense core vesicles in the perinuclear region.

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“…An equivalent amount of serotonin is secreted by the other Retzius neuron in the ganglion, since both respond in parallel upon the activation of common synaptic inputs (Velázquez-Ulloa et al, 2003). Although several questions still remain open, it is not surprising that a neuron pair is capable of producing the multiple modulatory effects of serotonin seen in the leech (Willard, 1981; Kristan and JrNusbaum, 1982; Burrell et al, 2002; Crisp and Mesce, 2006; Calviño and Szczupak, 2008; Bisson and Torre, 2011). …”

Section: Serotoninmentioning

confidence: 99%

Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system

Trueta¹,

De‐Miguel²

2012

Front. Physio.

103

127

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We review the evidence of exocytosis from extrasynaptic sites in the soma, dendrites, and axonal varicosities of central and peripheral neurons of vertebrates and invertebrates, with emphasis on somatic exocytosis, and how it contributes to signaling in the nervous system. The finding of secretory vesicles in extrasynaptic sites of neurons, the presence of signaling molecules (namely transmitters or peptides) in the extracellular space outside synaptic clefts, and the mismatch between exocytosis sites and the location of receptors for these molecules in neurons and glial cells, have long suggested that in addition to synaptic communication, transmitters are released, and act extrasynaptically. The catalog of these molecules includes low molecular weight transmitters such as monoamines, acetylcholine, glutamate, gama-aminobutiric acid (GABA), adenosine-5-triphosphate (ATP), and a list of peptides including substance P, brain-derived neurotrophic factor (BDNF), and oxytocin. By comparing the mechanisms of extrasynaptic exocytosis of different signaling molecules by various neuron types we show that it is a widespread mechanism for communication in the nervous system that uses certain common mechanisms, which are different from those of synaptic exocytosis but similar to those of exocytosis from excitable endocrine cells. Somatic exocytosis has been measured directly in different neuron types. It starts after high-frequency electrical activity or long experimental depolarizations and may continue for several minutes after the end of stimulation. Activation of L-type calcium channels, calcium release from intracellular stores and vesicle transport towards the plasma membrane couple excitation and exocytosis from small clear or large dense core vesicles in release sites lacking postsynaptic counterparts. The presence of synaptic and extrasynaptic exocytosis endows individual neurons with a wide variety of time- and space-dependent communication possibilities. Extrasynaptic exocytosis may be the major source of signaling molecules producing volume transmission and by doing so may be part of a long duration signaling mode in the nervous system.

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Spatial-specific action of serotonin within the leech midbody ganglion

Cited by 12 publications

References 48 publications

Functional integration of a serotonergic neuron in the Drosophila antennal lobe

Functional integration of a serotonergic neuron in the Drosophila antennal lobe

Cycling of Dense Core Vesicles Involved in Somatic Exocytosis of Serotonin by Leech Neurons

Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system

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