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Anatomical Organization of Multiple Modulatory Inputs in a Rhythmic Motor System.

Swallie SE, Monti AM, Blitz DM - PLoS ONE (2015)

Bottom Line: The POC neuron terminals form a defined neuroendocrine organ (anterior commissural organ: ACO) that utilizes peptidergic paracrine signaling to act on MCN1.The MCN1 arborization consistently coincided with the ACO structure, despite morphological variation between preparations.Contrary to a previous 2D study, our 3D analysis revealed that GPR axons did not terminate in a compact bundle, but arborized more extensively near MCN1, arguing against sparse connectivity of GPR onto MCN1.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Miami University, Oxford, OH, United States of America.

ABSTRACT
In rhythmic motor systems, descending projection neuron inputs elicit distinct outputs from their target central pattern generator (CPG) circuits. Projection neuron activity is regulated by sensory inputs and inputs from other regions of the nervous system, relaying information about the current status of an organism. To gain insight into the organization of multiple inputs targeting a projection neuron, we used the identified neuron MCN1 in the stomatogastric nervous system of the crab, Cancer borealis. MCN1 originates in the commissural ganglion and projects to the stomatogastric ganglion (STG). MCN1 activity is differentially regulated by multiple inputs including neuroendocrine (POC) and proprioceptive (GPR) neurons, to elicit distinct outputs from CPG circuits in the STG. We asked whether these defined inputs are compact and spatially segregated or dispersed and overlapping relative to their target projection neuron. Immunocytochemical labeling, intracellular dye injection and three-dimensional (3D) confocal microscopy revealed overlap of MCN1 neurites and POC and GPR terminals. The POC neuron terminals form a defined neuroendocrine organ (anterior commissural organ: ACO) that utilizes peptidergic paracrine signaling to act on MCN1. The MCN1 arborization consistently coincided with the ACO structure, despite morphological variation between preparations. Contrary to a previous 2D study, our 3D analysis revealed that GPR axons did not terminate in a compact bundle, but arborized more extensively near MCN1, arguing against sparse connectivity of GPR onto MCN1. Consistent innervation patterns suggest that integration of the sensory GPR and peptidergic POC inputs occur through more distributed and more tightly constrained anatomical interactions with their common modulatory projection neuron target than anticipated.

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Schematic of the isolated STNS including the projection neuron MCN1, the sensory neurons GPR1/2, and the POC neurons.There is a single MCN1 (blue) cell body in each CoG that projects to the STG. The POC neurons (red) originate outside of the STNS and enter the CoG to terminate as a neuroendocrine organ, the ACO. The somata of the two bilateral pairs of GPR neurons (green) occur in peripheral nerves. These bipolar neurons terminate in muscles and project anteriorly to the STG and continue into the CoGs. Abbreviations: Ganglia- CoG, commissural ganglion; OG, oesophageal ganglion; SOG, supraoesophageal ganglion; STG, stomatogastric ganglion; TG, thoracic ganglion. Neurons- GPR, gastropyloric receptor neuron; MCN1, modulatory commissural neuron 1; POC, post-oesophageal commissure neurons. Nerves: coc, circumoesophageal connective; dgn, dorsal gastric nerve; gpn, gastropyloric nerve; ion, inferior oesophageal nerve; lgn, lateral gastric nerve; lvn, lateral ventricular nerve; mgn, medial gastric nerve; mvn, medial ventricular nerve; poc, post-oesophageal commissure; son, superior oesophageal nerve; stn, stomatogastric nerve. Other: ACO, anterior commissural organ.
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pone.0142956.g001: Schematic of the isolated STNS including the projection neuron MCN1, the sensory neurons GPR1/2, and the POC neurons.There is a single MCN1 (blue) cell body in each CoG that projects to the STG. The POC neurons (red) originate outside of the STNS and enter the CoG to terminate as a neuroendocrine organ, the ACO. The somata of the two bilateral pairs of GPR neurons (green) occur in peripheral nerves. These bipolar neurons terminate in muscles and project anteriorly to the STG and continue into the CoGs. Abbreviations: Ganglia- CoG, commissural ganglion; OG, oesophageal ganglion; SOG, supraoesophageal ganglion; STG, stomatogastric ganglion; TG, thoracic ganglion. Neurons- GPR, gastropyloric receptor neuron; MCN1, modulatory commissural neuron 1; POC, post-oesophageal commissure neurons. Nerves: coc, circumoesophageal connective; dgn, dorsal gastric nerve; gpn, gastropyloric nerve; ion, inferior oesophageal nerve; lgn, lateral gastric nerve; lvn, lateral ventricular nerve; mgn, medial gastric nerve; mvn, medial ventricular nerve; poc, post-oesophageal commissure; son, superior oesophageal nerve; stn, stomatogastric nerve. Other: ACO, anterior commissural organ.

Mentions: The crustacean stomatogastric nervous system (STNS) enables a cellular level analysis of CPG function and its modulation using identified neurons [12,20]. Projection neurons activate and modulate CPGs, located in the stomatogastric ganglion (STG), which underlie the chewing and filtering of food (Fig 1) [12,21]. The majority of these projection neurons originate in the CoGs (commissural ganglia) with somata located near the surface and neuropil located more centrally [22–24]. The CoGs protrude from the circumoesophageal connectives (cocs) connecting the supraoesophageal ganglion (SOG) and the thoracic ganglion (TG) (Fig 1) [22]. Each CoG contains several hundred cells with overlapping distributions of somata projecting to the SOG (~50), to the TG (~100) and to the STG (~20) [23,25,26]. Among the ~20 projection neurons to the STG, a subset have been identified, their influence on STG circuits characterized, and several of their inputs identified [12,27–29]. However, the anatomical organization of inputs to identified projection neurons has not been examined.


Anatomical Organization of Multiple Modulatory Inputs in a Rhythmic Motor System.

Swallie SE, Monti AM, Blitz DM - PLoS ONE (2015)

Schematic of the isolated STNS including the projection neuron MCN1, the sensory neurons GPR1/2, and the POC neurons.There is a single MCN1 (blue) cell body in each CoG that projects to the STG. The POC neurons (red) originate outside of the STNS and enter the CoG to terminate as a neuroendocrine organ, the ACO. The somata of the two bilateral pairs of GPR neurons (green) occur in peripheral nerves. These bipolar neurons terminate in muscles and project anteriorly to the STG and continue into the CoGs. Abbreviations: Ganglia- CoG, commissural ganglion; OG, oesophageal ganglion; SOG, supraoesophageal ganglion; STG, stomatogastric ganglion; TG, thoracic ganglion. Neurons- GPR, gastropyloric receptor neuron; MCN1, modulatory commissural neuron 1; POC, post-oesophageal commissure neurons. Nerves: coc, circumoesophageal connective; dgn, dorsal gastric nerve; gpn, gastropyloric nerve; ion, inferior oesophageal nerve; lgn, lateral gastric nerve; lvn, lateral ventricular nerve; mgn, medial gastric nerve; mvn, medial ventricular nerve; poc, post-oesophageal commissure; son, superior oesophageal nerve; stn, stomatogastric nerve. Other: ACO, anterior commissural organ.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4643987&req=5

pone.0142956.g001: Schematic of the isolated STNS including the projection neuron MCN1, the sensory neurons GPR1/2, and the POC neurons.There is a single MCN1 (blue) cell body in each CoG that projects to the STG. The POC neurons (red) originate outside of the STNS and enter the CoG to terminate as a neuroendocrine organ, the ACO. The somata of the two bilateral pairs of GPR neurons (green) occur in peripheral nerves. These bipolar neurons terminate in muscles and project anteriorly to the STG and continue into the CoGs. Abbreviations: Ganglia- CoG, commissural ganglion; OG, oesophageal ganglion; SOG, supraoesophageal ganglion; STG, stomatogastric ganglion; TG, thoracic ganglion. Neurons- GPR, gastropyloric receptor neuron; MCN1, modulatory commissural neuron 1; POC, post-oesophageal commissure neurons. Nerves: coc, circumoesophageal connective; dgn, dorsal gastric nerve; gpn, gastropyloric nerve; ion, inferior oesophageal nerve; lgn, lateral gastric nerve; lvn, lateral ventricular nerve; mgn, medial gastric nerve; mvn, medial ventricular nerve; poc, post-oesophageal commissure; son, superior oesophageal nerve; stn, stomatogastric nerve. Other: ACO, anterior commissural organ.
Mentions: The crustacean stomatogastric nervous system (STNS) enables a cellular level analysis of CPG function and its modulation using identified neurons [12,20]. Projection neurons activate and modulate CPGs, located in the stomatogastric ganglion (STG), which underlie the chewing and filtering of food (Fig 1) [12,21]. The majority of these projection neurons originate in the CoGs (commissural ganglia) with somata located near the surface and neuropil located more centrally [22–24]. The CoGs protrude from the circumoesophageal connectives (cocs) connecting the supraoesophageal ganglion (SOG) and the thoracic ganglion (TG) (Fig 1) [22]. Each CoG contains several hundred cells with overlapping distributions of somata projecting to the SOG (~50), to the TG (~100) and to the STG (~20) [23,25,26]. Among the ~20 projection neurons to the STG, a subset have been identified, their influence on STG circuits characterized, and several of their inputs identified [12,27–29]. However, the anatomical organization of inputs to identified projection neurons has not been examined.

Bottom Line: The POC neuron terminals form a defined neuroendocrine organ (anterior commissural organ: ACO) that utilizes peptidergic paracrine signaling to act on MCN1.The MCN1 arborization consistently coincided with the ACO structure, despite morphological variation between preparations.Contrary to a previous 2D study, our 3D analysis revealed that GPR axons did not terminate in a compact bundle, but arborized more extensively near MCN1, arguing against sparse connectivity of GPR onto MCN1.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Miami University, Oxford, OH, United States of America.

ABSTRACT
In rhythmic motor systems, descending projection neuron inputs elicit distinct outputs from their target central pattern generator (CPG) circuits. Projection neuron activity is regulated by sensory inputs and inputs from other regions of the nervous system, relaying information about the current status of an organism. To gain insight into the organization of multiple inputs targeting a projection neuron, we used the identified neuron MCN1 in the stomatogastric nervous system of the crab, Cancer borealis. MCN1 originates in the commissural ganglion and projects to the stomatogastric ganglion (STG). MCN1 activity is differentially regulated by multiple inputs including neuroendocrine (POC) and proprioceptive (GPR) neurons, to elicit distinct outputs from CPG circuits in the STG. We asked whether these defined inputs are compact and spatially segregated or dispersed and overlapping relative to their target projection neuron. Immunocytochemical labeling, intracellular dye injection and three-dimensional (3D) confocal microscopy revealed overlap of MCN1 neurites and POC and GPR terminals. The POC neuron terminals form a defined neuroendocrine organ (anterior commissural organ: ACO) that utilizes peptidergic paracrine signaling to act on MCN1. The MCN1 arborization consistently coincided with the ACO structure, despite morphological variation between preparations. Contrary to a previous 2D study, our 3D analysis revealed that GPR axons did not terminate in a compact bundle, but arborized more extensively near MCN1, arguing against sparse connectivity of GPR onto MCN1. Consistent innervation patterns suggest that integration of the sensory GPR and peptidergic POC inputs occur through more distributed and more tightly constrained anatomical interactions with their common modulatory projection neuron target than anticipated.

Show MeSH
Related in: MedlinePlus