NeuroFIG 6: VNC motor neurons and locomotory circuit.
A. Neuronal control of locomotion during sensory and exploratory behaviors. (Left panel) The forward locomotion of the animal is interrupted by occasional turns and brief reversals. Omega turns result in an approximately 180°change in the direction of movement and usually follow a reversal. They can be spontaneous during exploration or induced by aversive stimuli. In the circuits that lead to reversals and turns, the dotted arrows indicate polysynaptic input. (Right panel) Mechanosensory reflex circuit (escape circuit). Five mechanosensory neurons (pink) that detect touch stimuli synapse onto command interneurons (red). These, in turn, synapse onto motor neurons (purple) responsible for forward (Fo) and backward (Ba) locomotion, leading to rapid withdrawal from the stimulus. Spontaneous forward motion can be initiated by a head motor nervous system, which is partially independent of the command interneurons (Chalfie et al., 1985; Zheng et al., 1999). DVA is a stretch-sensitive neuron with input to command interneurons and has a role in maintenance of the overall activity of the circuit (Li et al. 2006.) The neuronal circuit that controls locomotion has been dissected into two parts by laser-ablation studies of command interneurons; PVC and AVB are primarily required for promoting forward movement, and AVA, AVD, and AVE are for backward movement (Chalfie et al., 1985). AVB makes gap junctions, and PVC makes chemical synapses with B motor neurons, which drive forward motion. AVA and AVD synapse, chemically and electrically, with class A motor neurons, which drive backward motion (A motor neurons also receive input from AVE in the anterior half of the body). Within the mechanosensory reflex circuit, ALM makes gap junctions to AVM in the NR, and ALM and AVM make gap junctions to AVD, which responds to touch stimuli applied to the anterior part of the animal (Driscoll and Kaplan, 1997). At hatching, ALM works by itself through AVD, and in late larval stages AVM is added into the circuit. PLMs make gap junctions to PVC, which is important for the posterior touch response. Touch neurons activate one circuit while inhibiting the other; ALM and AVM form inhibitory chemical synapses onto PVC, and PLM forms inhibitory chemical synapses onto AVD, thus preventing inadvertent opposite locomotion in the reflex cycle. This circuit also receives input from head mechanosensory receptor neurons (not shown).
B. The A motor neurons control backward locomotion and B motor neurons control forward locomotion. D motor neurons, which receive synapses from A and B motor neurons and function as cross-inhibitory on the body wall muscles, are required for both forward and backward locomotion. On the dorsal side, VDs are exclusively post-synaptic, receiving input from DA, DB, and AS neurons as corecipients at neuromuscular junctions (NMJs) (dyadic synapse). On the ventral side, VD neurons are presynaptic to body wall muscle. DDs are exclusively post-synaptic on the ventral side, where they receive input from VA, VB, and VC neurons as corecipients at NMJs (dyadic synapse). DDs are predominantly presynaptic to body wall muscle on the dorsal side. The synaptic zones for the members of each class do not overlap, creating a clearly defined fate map of neuromuscular activity for each class (White et al., 1976). VC neurons are an exception to this rule. Active zones of members of different classes overlap; however, the transition regions among members are not generally the same for every class (White et al., 1976; Von Stetina et al., 2006). Neurons of a given class, except for VA, are electrically coupled to one another via gap junctions in both the VNC and DC. Similarly, muscle cells in each row of a muscle quadrant are also electrically coupled to their neighbors. The boxed model shows how reciprocal inhibitors (DD, VD) receive inputs diametrically opposite to their zone of innervation, so that contracting muscle quadrants (+) are matched by relaxing quadrants (–) on the opposite side of the body. (S) Synapse-free stretch-sensitive regions; (vm) vulval muscle; (green ovals) muscle; (red lines) interneurons; (black arrows and arrowheads) excitatory chemical synapses; (T-shaped lines) inhibitory chemical synapses; (straight lines with bars on each side) gap junctions.
C. Schematic representation of positions of motor neurons between RVG and PAG along the VNC. (Based on White et al., 1976, 1986.)
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