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Localization of Motor Neurons and Central Pattern Generators for Motor Patterns Underlying Feeding Behavior in Drosophila Larvae.

Hückesfeld S, Schoofs A, Schlegel P, Miroschnikow A, Pankratz MJ - PLoS ONE (2015)

Bottom Line: Motor systems can be functionally organized into effector organs (muscles and glands), the motor neurons, central pattern generators (CPG) and higher control centers of the brain.By classical lesion experiments we localize a set of CPGs generating the neuronal pattern underlying feeding movements to the subesophageal zone (SEZ).These findings provide a basis for progressing upstream of the motor neurons to identify higher regulatory components of the feeding motor system.

View Article: PubMed Central - PubMed

Affiliation: LIMES-Institute, University of Bonn, 53115, Bonn, Germany.

ABSTRACT
Motor systems can be functionally organized into effector organs (muscles and glands), the motor neurons, central pattern generators (CPG) and higher control centers of the brain. Using genetic and electrophysiological methods, we have begun to deconstruct the motor system driving Drosophila larval feeding behavior into its component parts. In this paper, we identify distinct clusters of motor neurons that execute head tilting, mouth hook movements, and pharyngeal pumping during larval feeding. This basic anatomical scaffold enabled the use of calcium-imaging to monitor the neural activity of motor neurons within the central nervous system (CNS) that drive food intake. Simultaneous nerve- and muscle-recordings demonstrate that the motor neurons innervate the cibarial dilator musculature (CDM) ipsi- and contra-laterally. By classical lesion experiments we localize a set of CPGs generating the neuronal pattern underlying feeding movements to the subesophageal zone (SEZ). Lesioning of higher brain centers decelerated all feeding-related motor patterns, whereas lesioning of ventral nerve cord (VNC) only affected the motor rhythm underlying pharyngeal pumping. These findings provide a basis for progressing upstream of the motor neurons to identify higher regulatory components of the feeding motor system.

No MeSH data available.


Related in: MedlinePlus

Activation and inactivation of feeding related motor neurons leads to decline in feeding.A, Experimental setup: yeast intake of larvae at 18°C and 32°C (% of larval body stained with red yeast) was determined after 20min of TrpA1-activation and shiTS-inactivation. B, Fold change in yeast intake; in both cases no dyed food could be observed in experimental larvae. C, Inactivation by shiTS of glutamatergic neurons results in decline of cibarial dilator muscle (CDM) postsynaptic potentials (PSP), but not in the antennal nerve (AN) motor pattern. D, Activation of glutamatergic neurons via channelrhodopsin (UAS-ChR2(H134R) or inhibition via halorhodopsin (UAS-eNpHR) resulted in direct tonic excitation or complete inhibition of the AN motor pattern.
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pone.0135011.g005: Activation and inactivation of feeding related motor neurons leads to decline in feeding.A, Experimental setup: yeast intake of larvae at 18°C and 32°C (% of larval body stained with red yeast) was determined after 20min of TrpA1-activation and shiTS-inactivation. B, Fold change in yeast intake; in both cases no dyed food could be observed in experimental larvae. C, Inactivation by shiTS of glutamatergic neurons results in decline of cibarial dilator muscle (CDM) postsynaptic potentials (PSP), but not in the antennal nerve (AN) motor pattern. D, Activation of glutamatergic neurons via channelrhodopsin (UAS-ChR2(H134R) or inhibition via halorhodopsin (UAS-eNpHR) resulted in direct tonic excitation or complete inhibition of the AN motor pattern.

Mentions: The line OK371-Gal4 labels a large population of motor neurons, if not all, and neuronal activation using this line results in a tonic excitation pattern of AN and other pharyngeal nerves [20]. Since this Gal4-line also marks the feeding motor neurons, inhibiting OK371-Gal4 labelled neurons should lead to a decrease in food intake and an inhibition of muscle contraction. Therefore, we expressed shibireTS in glutamatergic neurons (OK371-Gal4 drives UAS- shibireTS), which blocks synaptic transmission upon shifting to restrictive temperature, and performed food intake assays as well as recording extracellularly from the AN and intracellularly from the CDM (Fig 5A–5C). We focused on the AN/CDM pair since it was technically more feasible to perform double recordings from the nerve and the innervated muscles.


Localization of Motor Neurons and Central Pattern Generators for Motor Patterns Underlying Feeding Behavior in Drosophila Larvae.

Hückesfeld S, Schoofs A, Schlegel P, Miroschnikow A, Pankratz MJ - PLoS ONE (2015)

Activation and inactivation of feeding related motor neurons leads to decline in feeding.A, Experimental setup: yeast intake of larvae at 18°C and 32°C (% of larval body stained with red yeast) was determined after 20min of TrpA1-activation and shiTS-inactivation. B, Fold change in yeast intake; in both cases no dyed food could be observed in experimental larvae. C, Inactivation by shiTS of glutamatergic neurons results in decline of cibarial dilator muscle (CDM) postsynaptic potentials (PSP), but not in the antennal nerve (AN) motor pattern. D, Activation of glutamatergic neurons via channelrhodopsin (UAS-ChR2(H134R) or inhibition via halorhodopsin (UAS-eNpHR) resulted in direct tonic excitation or complete inhibition of the AN motor pattern.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4529123&req=5

pone.0135011.g005: Activation and inactivation of feeding related motor neurons leads to decline in feeding.A, Experimental setup: yeast intake of larvae at 18°C and 32°C (% of larval body stained with red yeast) was determined after 20min of TrpA1-activation and shiTS-inactivation. B, Fold change in yeast intake; in both cases no dyed food could be observed in experimental larvae. C, Inactivation by shiTS of glutamatergic neurons results in decline of cibarial dilator muscle (CDM) postsynaptic potentials (PSP), but not in the antennal nerve (AN) motor pattern. D, Activation of glutamatergic neurons via channelrhodopsin (UAS-ChR2(H134R) or inhibition via halorhodopsin (UAS-eNpHR) resulted in direct tonic excitation or complete inhibition of the AN motor pattern.
Mentions: The line OK371-Gal4 labels a large population of motor neurons, if not all, and neuronal activation using this line results in a tonic excitation pattern of AN and other pharyngeal nerves [20]. Since this Gal4-line also marks the feeding motor neurons, inhibiting OK371-Gal4 labelled neurons should lead to a decrease in food intake and an inhibition of muscle contraction. Therefore, we expressed shibireTS in glutamatergic neurons (OK371-Gal4 drives UAS- shibireTS), which blocks synaptic transmission upon shifting to restrictive temperature, and performed food intake assays as well as recording extracellularly from the AN and intracellularly from the CDM (Fig 5A–5C). We focused on the AN/CDM pair since it was technically more feasible to perform double recordings from the nerve and the innervated muscles.

Bottom Line: Motor systems can be functionally organized into effector organs (muscles and glands), the motor neurons, central pattern generators (CPG) and higher control centers of the brain.By classical lesion experiments we localize a set of CPGs generating the neuronal pattern underlying feeding movements to the subesophageal zone (SEZ).These findings provide a basis for progressing upstream of the motor neurons to identify higher regulatory components of the feeding motor system.

View Article: PubMed Central - PubMed

Affiliation: LIMES-Institute, University of Bonn, 53115, Bonn, Germany.

ABSTRACT
Motor systems can be functionally organized into effector organs (muscles and glands), the motor neurons, central pattern generators (CPG) and higher control centers of the brain. Using genetic and electrophysiological methods, we have begun to deconstruct the motor system driving Drosophila larval feeding behavior into its component parts. In this paper, we identify distinct clusters of motor neurons that execute head tilting, mouth hook movements, and pharyngeal pumping during larval feeding. This basic anatomical scaffold enabled the use of calcium-imaging to monitor the neural activity of motor neurons within the central nervous system (CNS) that drive food intake. Simultaneous nerve- and muscle-recordings demonstrate that the motor neurons innervate the cibarial dilator musculature (CDM) ipsi- and contra-laterally. By classical lesion experiments we localize a set of CPGs generating the neuronal pattern underlying feeding movements to the subesophageal zone (SEZ). Lesioning of higher brain centers decelerated all feeding-related motor patterns, whereas lesioning of ventral nerve cord (VNC) only affected the motor rhythm underlying pharyngeal pumping. These findings provide a basis for progressing upstream of the motor neurons to identify higher regulatory components of the feeding motor system.

No MeSH data available.


Related in: MedlinePlus