Selective Inhibition Mediates the Sequential Recruitment of Motor Pools

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Abstract

Locomotor systems generate diverse motor patterns to produce the movements underlying behavior, requiring that motor neurons be recruited at various phases of the locomotor cycle. Reciprocal inhibition produces alternating motor patterns; however, the mechanisms that generate other phasic relationships between intrasegmental motor pools are unknown. Here, we investigate one such motor pattern in the Drosophila larva, using a multidisciplinary approach including electrophysiology and ssTEM-based circuit reconstruction. We find that two motor pools that are sequentially recruited during locomotion have identical excitable properties. In contrast, they receive input from divergent premotor circuits. We find that this motor pattern is not orchestrated by differential excitatory input but by a GABAergic interneuron acting as a delay line to the later-recruited motor pool. Our findings show how a motor pattern is generated as a function of the modular organization of locomotor networks through segregation of inhibition, a potentially general mechanism for sequential motor patterns.

Figures

  • Figure 1. Motor Neuron Intrinsic Properties Do Not Contribute to the Generation of the Intrasegmental Motor Pattern Underlying Larval Crawling (A) Longitudinal muscle LO1 (magenta) and transverse muscles LT1–LT4 (green) in a single segment of the Drosophila larva. Left panel shows GFP-labeled muscles of hemisegments A3–A5, schematized in the right panel. Scale bar, 200 mm. (B) Contraction pattern of LT2 and LO1 in segment A4 in (A) during a crawling cycle. (C) Polar plot of magnitude and phase of coherency of the two waveforms with LO1 as reference. Dashed line indicates a = 0.05 for coherence magnitude statistically deviating from 0. Data are represented as mean ± 95% confidence interval (CI). (D and E) Example motor neurons during patch-clamp recording from cell bodies (asterisks) labeled with Alexa Fluor 568 Hydrazide dye, pseudocolored green (D; MN-LT) or magenta (E; MN-LO1). Blue shading is mCD8::GFP expression under the B-H1 promoter. Scale bar in (E), 5 mm. (F and G) Example recordings of MN-LT (F) and MN-LO1 (G) during different levels of current injection. (H–K) (H) Capacitance (Cm), (I) membrane resistance (Rm), (J) membrane voltage threshold to action potential (Vm threshold), and (K) resting membrane potential (Vm rest) of MN-LTs (green) and MN-LO1s (magenta). Boxplots show mean ± quartiles; whiskers minimum to maximum value. p > 0.05, t tests. (L and M) The number of action potentials (L) and delay to first spike (M) as a function of the amplitude of current injection for MN-LTs (green) and MN-LO1s (magenta). There is no statistically significant difference between the slopes of the linear regression lines in (L) (p > 0.05), and one curve fits best the non-linear fit in (M). n = 9 for MN-LTs; n = 5 for MN-LO1. Also see Figure S1.
  • Figure 2. Functionally Distinct Motor Neurons Receive Divergent Input
  • Figure 3. eIN-1 Innervates Transverse Motor Neurons and Is Recruited in Phase with Longitudinal Output in the Same Segment
  • Figure 4. The Intrasegmental Motor Pattern Is Sensitive to PTX
  • Figure 5. iIN-1 Specifically Innervates Transverse Motor Neurons and Shows Wave-like Activity during Fictive Locomotion
  • Figure 6. The Output of iIN-1 Is Required to Generate the Intrasegmental Motor Pattern

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CITATION STYLE

APA

Zwart, M. F., Pulver, S. R., Truman, J. W., Fushiki, A., Fetter, R. D., Cardona, A., & Landgraf, M. (2016). Selective Inhibition Mediates the Sequential Recruitment of Motor Pools. Neuron, 91(3), 615–628. https://doi.org/10.1016/j.neuron.2016.06.031

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