Modulation of spontaneous and reflex activity of crayfish leg motor neurons by octopamine and serotonin.

Abstract

1. We compared the effects of octopamine and serotonin on the activity of crayfish leg motor neurons in an isolated preparation of the 4th thoracic ganglion. Spontaneous activity of leg promotor (swing phase in a forward walking crayfish) and remotor (stance phase) motor neurons consisted either of continuous promotor activity (with the remotor nerve silent) or alternating bursts of promotor and remotor activity. Octopamine and serotonin, at high concentrations (< or = 100 and < or = 20 microM, respectively), abolished spontaneous promotor activity and rhythmic bursting (if ongoing). Both amines induced tonic remotor nerve activity, but each amine activated different identified remotor motor neurons. 2. Reflex responses of remotor motor neurons to stimulation of thoracocoxal (TC) joint proprioceptors were modulated by octopamine and serotonin in characteristic ways. The muscle receptor (TCMRO) that signals joint remotion excited a subset of remotor motor neurons in an assistance reflex. The chordotonal organ (TCCO) that signals joint promotion excited different remotor motor neurons in a resistance reflex. Octopamine abolished assistance reflexes and facilitated resistance reflexes. One assistance group unit was inhibited, whereas reflex reversal was induced in another: this unit was now excited in a resistance reflex, rather than in an assistance reflex. The responses of resistance group remotor units were enhanced. Serotonin had the opposite effect on assistance group remotors: one unit was excited and generated a stronger assistance reflex. The effect of serotonin on resistance group remotor units was similar (but quantitatively different) to that of octopamine. 3. Both octopamine and serotonin modulated spontaneous motor output at concentrations below those required to inhibit promotor nerve activity. Rhythmic promotor and remotor bursting was abolished, and replaced with continuous promotor activity, by serotonin at 1 microM and octopamine at 1-10 microM. In nonbursting preparations, promotor activity could be excited (instead of inhibited) by either amine at lower concentrations. 4. Octopaminergic inhibition of spontaneous promotor activity was antagonized by mianserin (10 microM). Phentolamine at the same concentration was less effective as an antagonist. Serotonergic inhibition of promotor activity was not blocked by mianserin. Mianserin also antagonized inhibitory, but not excitatory, effects of octopamine on remotor reflex responses. Serotonergic modulation of these reflexes was not affected. 5. An intersegmental difference was found in aminergic inhibition of promotor nerve activity. Whereas the effect (at the higher concentrations used) was inhibition of promotor activity from T4, simultaneous recordings from promotor nerves of the more rostral ganglia T3 and T2 showed either promotor excitation, or inhibition that was significantly weaker than in T4. This may relate to the known postural effects of these amines in intact crayfish and lobsters. 6. We conclude that octopamine and serotonin are modulators of segmental reflexes in the crayfish walking system. Each amine "assembles" a unique remotor nerve reflex response from different combinations of remotor units. In the case of octopamine, inhibitory effects are mediated by a mianserin-sensitive receptor, whereas excitatory effects are mediated by a mianserin-insensitive receptor.