Limits...
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.

Show MeSH

Related in: MedlinePlus

The ACO consistently occurs in the anterior region of the CoG.(A) A single optical slice including fluorescence signal (green: CabTRP Ia-IR) and DIC optics demonstrates that the ACO (filled arrowhead) was located in the anterior region of the CoG. (B) A volume rendering (170 slices, 1.0 μm interval) of the same ganglion as in (A) illustrates that the POC axons (open arrowhead) entered the CoG from the anterior coc and terminated as the large ACO structure (filled arrowhead). White line marks the edge of the CoG visible in (A). Scale bars: 100 μm. (C) The average location of the ACO indicates a consistent occurrence in the anterior portion but a variable location across the mediolateral axis. The ACO location is reported as the average (dark green center box) and standard deviation (lighter green center box) of the center of the ACO and the average (dark green filled outer box) and standard deviation (lighter green outer box) of the spread of the arborization as measured vertically and horizontally from center. coc, circumoesophageal connective; ion, inferior oesophageal nerve; son, superior oesophageal nerve.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4643987&req=5

pone.0142956.g004: The ACO consistently occurs in the anterior region of the CoG.(A) A single optical slice including fluorescence signal (green: CabTRP Ia-IR) and DIC optics demonstrates that the ACO (filled arrowhead) was located in the anterior region of the CoG. (B) A volume rendering (170 slices, 1.0 μm interval) of the same ganglion as in (A) illustrates that the POC axons (open arrowhead) entered the CoG from the anterior coc and terminated as the large ACO structure (filled arrowhead). White line marks the edge of the CoG visible in (A). Scale bars: 100 μm. (C) The average location of the ACO indicates a consistent occurrence in the anterior portion but a variable location across the mediolateral axis. The ACO location is reported as the average (dark green center box) and standard deviation (lighter green center box) of the center of the ACO and the average (dark green filled outer box) and standard deviation (lighter green outer box) of the spread of the arborization as measured vertically and horizontally from center. coc, circumoesophageal connective; ion, inferior oesophageal nerve; son, superior oesophageal nerve.

Mentions: The CabTRP Ia immunoreactive axons entering the CoG through the anterior coc arise from neurons named after their projection through the post-oesophageal commissure (poc: POC neurons), while their terminals form a neuroendocrine organ called the anterior commissural organ (ACO) based on its location within the CoG [28,34]. We maintain this nomenclature, referring to the axons as POC and the axon terminals that comprise the neuroendocrine organ as ACO. To determine the consistency of the ACO location within the CoG, we quantified its location relative to the margins of the CoG. A single optical slice combining DIC optics with CabTRP Ia-IR illustrates that the ACO was located close to the anterior CoG boundary (Fig 4). This optical slice contained the widest portion of the ACO. A volume rendering of a z-stack reveals that the POC axons entered the CoG from the anterior coc and terminated as the ACO, which arborized entirely within the anterior CoG (Fig 4B). In 14/14 preparations, the ACO was consistently contained in the anterior half of the CoG, while it spread across a large extent of the mediolateral CoG axis (Fig 4C).


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

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

The ACO consistently occurs in the anterior region of the CoG.(A) A single optical slice including fluorescence signal (green: CabTRP Ia-IR) and DIC optics demonstrates that the ACO (filled arrowhead) was located in the anterior region of the CoG. (B) A volume rendering (170 slices, 1.0 μm interval) of the same ganglion as in (A) illustrates that the POC axons (open arrowhead) entered the CoG from the anterior coc and terminated as the large ACO structure (filled arrowhead). White line marks the edge of the CoG visible in (A). Scale bars: 100 μm. (C) The average location of the ACO indicates a consistent occurrence in the anterior portion but a variable location across the mediolateral axis. The ACO location is reported as the average (dark green center box) and standard deviation (lighter green center box) of the center of the ACO and the average (dark green filled outer box) and standard deviation (lighter green outer box) of the spread of the arborization as measured vertically and horizontally from center. coc, circumoesophageal connective; ion, inferior oesophageal nerve; son, superior oesophageal nerve.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643987&req=5

pone.0142956.g004: The ACO consistently occurs in the anterior region of the CoG.(A) A single optical slice including fluorescence signal (green: CabTRP Ia-IR) and DIC optics demonstrates that the ACO (filled arrowhead) was located in the anterior region of the CoG. (B) A volume rendering (170 slices, 1.0 μm interval) of the same ganglion as in (A) illustrates that the POC axons (open arrowhead) entered the CoG from the anterior coc and terminated as the large ACO structure (filled arrowhead). White line marks the edge of the CoG visible in (A). Scale bars: 100 μm. (C) The average location of the ACO indicates a consistent occurrence in the anterior portion but a variable location across the mediolateral axis. The ACO location is reported as the average (dark green center box) and standard deviation (lighter green center box) of the center of the ACO and the average (dark green filled outer box) and standard deviation (lighter green outer box) of the spread of the arborization as measured vertically and horizontally from center. coc, circumoesophageal connective; ion, inferior oesophageal nerve; son, superior oesophageal nerve.
Mentions: The CabTRP Ia immunoreactive axons entering the CoG through the anterior coc arise from neurons named after their projection through the post-oesophageal commissure (poc: POC neurons), while their terminals form a neuroendocrine organ called the anterior commissural organ (ACO) based on its location within the CoG [28,34]. We maintain this nomenclature, referring to the axons as POC and the axon terminals that comprise the neuroendocrine organ as ACO. To determine the consistency of the ACO location within the CoG, we quantified its location relative to the margins of the CoG. A single optical slice combining DIC optics with CabTRP Ia-IR illustrates that the ACO was located close to the anterior CoG boundary (Fig 4). This optical slice contained the widest portion of the ACO. A volume rendering of a z-stack reveals that the POC axons entered the CoG from the anterior coc and terminated as the ACO, which arborized entirely within the anterior CoG (Fig 4B). In 14/14 preparations, the ACO was consistently contained in the anterior half of the CoG, while it spread across a large extent of the mediolateral CoG axis (Fig 4C).

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