Coordination and Modulation of Locomotion Pattern Generators inDrosophilaLarvae: Effects of Altered Biogenic Amine Levels by the Tyramine β Hydroxlyase Mutation

Abstract

Forward locomotion of Drosophila melanogaster larvae is composed of rhythmic waves of contractions that are thought to be produced by segmentally organized central pattern generators. We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wild-type and mutant larval preparations. We have shown previously that T␤h nM18 mutants, with altered levels of octopamine and tyramine, have a locomotion deficit. By recording en passant from the segmental nerves, we investigated the coordination of the neuronal activity driving contraction waves of the abdominal body-wall muscles. Rhythmic bursts of activity that occurred concurrently with locomotive waves were frequently observed in wild-type larvae but were rarely seen in T␤h nM18 mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and T␤h nM18 larvae after severing the segmental nerve from the CNS. Patterned activities persisted in the proximal stumps deprived of sensory feedback from the periphery. Simultaneous recordings demonstrated a delay in the bursting activity between different segments, with greater delay for segments that were farther apart. In contrast, bilateral recordings within a single segment revealed a well synchronized activity pattern in nerves innervating each hemisegment in both wild-type and T␤h nM18 larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in T␤h nM18 mutants by head or tail stimulation despite their highly irregular spontaneous activities. These observations suggest a role of the biogenic amines in the initiation and modulation of motor pattern generation. The technique presented here can be readily extended to examine the locomotion motor program of other mutants.

Distinct Frequency-Dependent Regulation of Nerve Terminal Excitability and Synaptic Transmission by IA and IK Potassium Channels Revealed by Drosophila Shaker and Shab Mutations

“…We further used a semi-intact larval neuromuscular preparation to monitor locomotor patterns of spike activities in segmental nerves that innervate the body wall muscles while observing corresponding muscle contraction waves along the body axis (Fox et al, 2006). In WT larvae, the motor pattern generated by the CNS drives a propagating wave of muscle contractions from posterior to anterior segments, corresponding to the forward crawling ( Fig.…”

“…The CNS and segmental nerves were maintained intact during larval dissection. Propagating waves of muscle contractions from posterior to anterior segments or from anterior to posterior segments were observed when the preparation was perfused with an HL3 saline containing 1.5 mM Ca 2ϩ (Stewart et al, 1994) at a rate of 0.5ϳ1 ml/min (Fox et al, 2006). Spontaneous, ongoing nerve activity was recorded en passant (Fox et al, 2006) using a suction electrode and a differential amplifier (DAM-5A; WPI) and was then displayed on a chart recorder (Gould 220; Gould, Cleveland, OH).…”

Neurogenetic networks for startle-induced locomotion in Drosophila melanogaster

“…In addition, association studies found polymorphisms associated with variation in startle-induced locomotion in Catsup, which encodes a negative regulator of tyrosine hydroxylase, the rate-limiting enzyme in the synthesis of dopamine (12), and in Ddc, which encodes dopamine decarboxylase (11). Additional studies in Drosophila have implicated serotonin, octopamine, and ␥-aminobutyric acid as critical mediators of locomotion (13)(14)(15)(16).…”

Plasticity and Second Messengers During Synapse Development

“…Unlike type I neurons which usually innervate a single muscle, type II synapses are widely distributed; three type II motor neurons in each segment provide synaptic input to all but 8 muscles of the body wall musculature (Monastirioti et al, 1995;Hoang and Chiba, 2001). These neurons therefore can provide broad modulation of the motor pattern (Fox et al, 2006).…”