Abstract
Descending pathways are important modulators of motor networks and allow the dynamic adjustment of behaviors to changing internal and external conditions. Central pattern generating networks (CPG) have been particularly amenable to study the modulation of motor networks and demonstrated that virtually all levels of information processing are controlled by descending projections. CPGs receive sensory feedback and while it is known that sensory activity can be gated by central pathways, we here present for the first time that descending projection neurons modulate action potential initiation in sensory neurons.
We used the fact that the anterior gastric receptor neuron (AGR), a single-cell bipolar muscle tendon organ in the crustacean stomatogastric nervous system, generates spontaneous ectopic action potentials in its axon. We found that axonal spike initiation is under direct neuromodulatory control by a pair of descending projection neurons. These IV (inferior ventricular) neurons descend from the brain and are known to control CPGs in the stomatogastric ganglion (STG). Activation of the IV neurons elicited a long-lasting decrease in AGR ectopic spike activity. This decrease was only observed when spikes were generated ectopically in the central portion of the axon, i.e. the modulation was specific to the site of spontaneous spike initiation. The decrease could be mimicked by focal application of the IV neuron co-transmitter histamine and IV neuron actions were diminished after blocking H2 receptors, indicating a direct descending modulation of the axonal spike initiation site. In contrast, the propagation dynamics of en-passant action potentials were not affected. Descending modulatory projection neurons therefore control axonal spike initiation in sensory neurons without affecting afferent spike propagation to increase the physiological activity repertoire of sensory pathways.
