Neural mechanisms of reflex reversal in coxo-basipodite depressor motor neurons of the crayfish.

The in vitro preparation of the fifth thoracic ganglion of the crayfish was used to investigate the mechanisms underlying the reflex reversal in a sensory-motor pathway. Sensory afferent neurons from the coxo-basipodite chordotonal organ (CBCO), which senses vertical movements of the limb, connect monosynaptically with basal limb motor neurons (MNs). In tonically active preparation, stretching the CBCO (corresponding to downward movements of the leg) stimulates the levator MNs, whereas releasing the CBCO activates the depressor (Dep) MNs. These reflexes, opposed to the imposed movement, are termed resistance reflexes. By contrast, during fictive locomotion, the reflexes are reversed and termed assistance reflexes. Intracellular recordings from all 12 Dep MNs were performed in single experiments. It allowed us to characterize three types of Dep MNs according to their response to CBCO imposed step-and-ramp movements: 8 of the 12 Dep MNs are resistance MNs that are depolarized during release of the CBCO and are connected monosynaptically to release-sensitive CBCO neurons; 1 Dep MN is an assistance MN that is depolarized during stretching of the CBCO and is connected monosynaptically to exclusively velocity-coding stretch-sensitive CBCO neurons; in our experimental conditions, 3 Dep MNs do not display any response to CBCO stimulation. Assistance reflex interneurons (ARINs), involved in polysynaptic assistance reflexes recorded from depressor MNs, are presented. During low-velocity (0.05 mm/s) stretching ramps imposed on the CBCO, ARINs display compound excitatory postsynaptic potentials (EPSPs), whereas during high-velocity (0.25 mm/s) ramps, they display a mixed excitatory and inhibitory response. Whereas a single MN generally receives monosynaptic EPSPs from three to six CBCO neurons, ARINs receive monosynaptic EPSPs from up to eight velocity-coding stretch-sensitive CBCO neurons. In addition, ARINs receive disynaptic inhibitory phasic inputs from stretch-sensitive CBCO afferents. Injection of a depolarizing current pulse into ARINs elicits a fast transient voltage-dependent depolarization. Its time to peak decreases, and its peak amplitude increases with increasing current intensity. ARINs likely are to be connected directly to Dep MNs. The synaptic delay between these nonspiking ARINs and Dep MNs is short (<2 ms) and constant. The postsynaptic EPSP amplitude increases with increasing current pulse intensity injected into ARIN. The dual sensory control (excitatory and inhibitory) makes it likely that ARIN represents a key element in reflex reversal control.