PRESYNAPTIC INHIBITION IS MEDIATED BY HISTAMINE AND GABA IN THE CRUSTACEAN ESCAPE REACTION

1. Presynaptic inhibition of sensory transmission during the escape re action in Crustacea has been studied using an in vitro preparation of the crayfish thoracic ganglia. Electrical stimulation of the medial gi ant fiber mediating the escape reaction induced depolarization in sens ory afferent terminals of the coxo-basal chordotonal organ (CBCO). Thi s depolarization was associated with an increase of the membrane condu ctance and was partially blocked by a gamma-aminobutyric acid (GABA) a ntagonist, picrotoxin, and by a histamine antagonist, cimetidine. 2. P ressure ejection of histamine on CBCO sensory terminals (CBT) recorded intracellularly, induced a depolarization of the membrane potential a ccompanied by a large increase of the conductance. Histamine-induced d epolarization persisted after blockade of synaptic transmission mediat ed by Na+ spikes by tetrodotoxin. The amplitude of histamine-induced d epolarization increased when negative current was injected into the se nsory terminal through the recording electrode. Moreover, injection of chloride into the CBT, which shifts the reversal potential of chlorid e to a more positive value, resulted in an increase of the amplitude o f the histamine-induced depolarization. 3. The existence of separate r eceptors for GABA and histamine on the CB sensory terminals was demons trated using two complementary sets of experiments. The first one cons isted of using specific blockers of GABA and histamine. Picrotoxin blo cked selectively the GABA-induced depolarization of the CB sensory ter minals, while it was ineffective in blocking the histamine-induced dep olarization. Conversely, cimetidine blocked the histamine-induced depo larization totally, but did not affect the GABA response. The second s et of experiments tested for of cross-desensitization between GABA and histamine responses. After desensitization of GABA response, histamin e was still able to produce depolarization in the CBT. 4. The depolari zation induced by medial giant fiber stimulation as well as by histami ne was accompanied by a marked decrease of the amplitude of the affere nt spikes recorded in the CB sensory terminals. This effect appeared, at least partially, to be mediated by a shunting mechanism due to the increased conductance during the depolarization. The effect of histami ne on synaptic transmission was also investigated by recording monosyn aptic excitatory postsynaptic potentials (EPSPs) induced in postsynapt ic motoneurons by electrical stimulation of the CB sensory nerve. Loca l application of histamine over the sensory terminals induced a marked decrease of the amplitude of the monosynaptic EPSPs. The effect of hi stamine is, thus, mainly mediated by a presynaptic inhibition because neither the membrane potential nor the input resistance of the motoneu rons were affected when histamine was applied. 5. In conclusion, the e scape reaction mediated by the medial giant fibers involves presynapti c inhibition of the CB sensory afferents, which is mediated by a simul taneous activation of both histamine and GABA receptors, in contrast t o the locomotor-related presynaptic inhibition, which is mediated by G ABA.