Presynaptic inhibition in the crayfish CNS: pathways and synaptic mechanisms

Abstract

I studied the pathways that produce primary afferent depolarization (PAD) and presynaptic inhibition during crayfish escape behavior. Simultaneous intracellular recordings were obtained from interneurons and primary afferent axons in the neuropil of the sixth abdominal ganglion. In several experiments, a sucrose-gap recording of PAD accompanied the intracellular impalements. I have identified PAD-producing inhibitory interneurons (PADIs) that are fired by a single impulse in the lateral (LG) or medial (MG) giant, escape-command axons; the PADIs appear to be directly responsible for presynaptic inhibition of primary afferent input to identified mechanosensory interneurons. PADI spikes, elicited by injection of depolarizing current, produced unitary PAD with constant short latency (mean = 0.97 +/- 0.12 SD ms). The unitary PADs were capable of following PADI impulses one for one at frequencies greater than 100 Hz, and the amplitude of unitary PAD was increased by injection of chloride into the afferent terminals. Therefore, the PADIs appear to directly produce an increase in chloride conductance in the primary afferent terminals. Intracellular injections of Lucifer yellow or horseradish peroxidase (HRP) revealed three morphological types of PADI. Their axonal branches and terminals are bilateral and overlap extensively with the innervation fields of all 10 sensory roots of the sixth ganglion. The three morphological types of PADI were physiologically indistinguishable. In several cases, the impaled PADI was shown to produce unitary PAD in more than one afferent of a given root as well as in afferents of adjacent roots. Therefore, the PADIs appear to diverge widely and contact many afferents in all of the sixth-ganglion sensory roots. Stimulation, caudal to the fifth ganglion, of an MG that had been interrupted rostral to the fifth ganglion produced no PAD in sixth-ganglion afferents. Also, stimulation of an MG or an LG in a surgically isolated sixth abdominal ganglion failed to produce PAD. Therefore, the pathway between the MGs and PADIs is activated exclusively within the rostral abdominal ganglia. Direct stimulation in the second and third abdominal ganglia of the segmental giants (SGs) produced a polysynaptic, suprathreshold response in the PADIs. This response was compound and was not due to the activity of the identified corollary discharge interneurons, CDI-2 and CDI-3, that are fired by the SGs. Therefore, the primary input to the PADIs must come from other, unidentified CDIs that are driven by the SGs. PADIs were not fired by shocks to the sensory portions of any peripheral roots even though these shocks produced PAD.(ABSTRACT TRUNCATED AT 400 WORDS)