The core of crawling: analysis of fictive motor patterns in the isolated Drosophila larval ventral nerve cord
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1
Janelia Farm Research Campus, Howard Hughes Medical Institute, United States
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2
University of Cambridge, Department of Zoology, United Kingdom
Locomotion in larval Drosophila has been the focus of numerous behavioral, electrophysiological and genetic studies; however, relatively little is known about the central pattern generating (CPG) circuits that form the core functional substrates for larval behaviors. Understanding the output of the larval locomotor CPG is a necessary first step towards understanding properties of underlying circuits. Here, we use a combination of behavioral analysis, functional imaging and electrophysiology to compare motor patterns in intact larvae to fictive motor patterns produced by isolated nerve cords in larval Drosophila.
Larval crawling is comprised primarily of posterior-to-anterior forward peristaltic waves of muscle contractions interspersed with ‘pause-turn’ episodes. First we examined inter-segmental coordination during bouts of forward crawling by tracking denticle band movements. Cycle periods of forward crawling vary from 0.6 s to 1.3 s in wild type animals. Across this range of cycle periods, the durations of contraction and retraction episodes scale linearly with cycle period. Next we examined inter-segmental coordination during pause-turns. Analysis of denticle band movements revealed that pause-turns are initiated by anterior-to-posterior backwards peristaltic waves that progress through anterior abdominal (A1-4) hemi-segments on one side of larvae.
To what extent are segmentally coordinated muscle contractions during crawling reflected in the output of larval CPG networks? To address this, we expressed the calcium indicator GCaMP3 in motor neurons and imaged rhythmic optical signals that correlate with segmental nerve activity in isolated ventral ganglia. 3rd instar animals generate segmentally coordinated motor patterns in the absence of sensory input; preparations show slow (>10s cycle period) bouts of bilaterally symmetric forward and backward persistalsis. Isolated nerve cords also show bilaterally asymmetric motor neuron activity in thoracic and anterior abdominal (A1-A4) segments. These asymmetries precede initiation of a majority of backward waves and show patterns of activity similar to those seen during pause-turns in behaving larvae. Surgical removal of the brain biased networks towards forward peristalsis while also decreasing cycle periods of forward waves. The effects of surgically removing subesophageal, thoracic and abdominal segments are currently under investigation.
This work shows that segmentally organized CPG networks in Drosophila larvae can endogenously produce a range of fictive motor patterns in an isolated nerve cord. It also suggests that in larvae, as in other animals (e.g. Mullins and Freisen, 2012) the brain adds variability and flexibility to the output of CPG networks. Overall, this work lays a foundation for future studies aimed at understanding principles governing how motor systems coordinate activity across many body segments.
*S.R.P. and T.G.B contributed equally to this work
Acknowledgements
This work was funded by grants from the Royal Society, the Wellcome Trust, the Newton Trust, the European Molecular Biology Organization, Downing College (University of Cambridge), and Janelia Farm Research Campus (Howard Hughes Medical Institute).
References
Mullins, O.J., Friesen, W.O. (2012) The brain matters: effects of descending signals on motor control. J. Neurophysiol. Epub ahead of print. Doi:10.1152/jn.00107.2012.
Keywords:
central pattern generators,
genetically encoded calcium indicators,
Neurogenetics
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for Participant Symposium)
Topic:
Motor Systems
Citation:
Pulver
SR,
Bayley
TG,
Taylor
AL,
Berni
J,
Bate
M and
Hedwig
B
(2012). The core of crawling: analysis of fictive motor patterns in the isolated Drosophila larval ventral nerve cord.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00417
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Received:
02 May 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Stefan R Pulver, Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA, 20147, United States, pulvers@janelia.hhmi.org