Octopamine induces steady-state reflex reversal in crayfish thoracic ganglia.

Abstract

1. This paper investigates the effect of octopamine on spontaneous and reflex motor output of crayfish leg motor neurons. Octopamine modulated spontaneous activity, both rhythmic and tonic, and dramatically modulated the pattern of reflex motor output elicited by stimulating identified proprioceptors of the basal limb. 2. Spontaneous reciprocal motor patterns, involving alternating bursts of promotor and remotor motor neuron activity, were reversibly abolished by octopamine. The threshold concentration for this effect was approximately 1 microM. 3. At concentrations greater than approximately 10 microM octopamine inhibited spontaneous promotor nerve activity in both bursting and nonbursting preparations. In some experiments promotor inhibition was correlated with the induction of tonic remotor nerve activity. The EC50 for complete inhibition of promotor nerve activity by octopamine was 20-30 microM. 4. Reflexes mediated by two basal limb proprioceptors, the thoracocoxal muscle receptor organ (TCMRO; which signals leg promotion) and the thoracocoxal chordotonal organ (TCCO; which signals leg remotion) were analyzed in a number of promotor and remotor motor neurons. In both cases assistance reflexes (excitation of promotors by the TCCO and remotors by the TCMRO) were restricted to subgroups of the motor pool. Among remotor motor neurons, the first two units recruited during bursts of spontaneous activity were members of the assistance reflex group (group 1). A third unit, sometimes recruited during more intense spontaneous bursts, was excited by TCCO stimulation and was therefore a member of the resistance reflex group (group 2). Other resistance group remotors were also excited by the TCCO, but this input normally remained subthreshold. 5. Stimulation of the TCCO afferent nerve elicited excitatory postsynaptic potentials (EPSPs) in group 2 (resistance group) remotor motor neurons at a latency compatible with a monosynaptic connection. The same stimulation excited group 1 (assistance group) promotor motor neurons, but at a greater and more variable latency. Thus the remotor resistance reflex from the TCCO is probably monosynaptic, but the promotor assistance reflex, also elicited by TCCO stimulation, is likely to be di- or polysynaptic. Assistance group (group 1) remotor motor neurons are inhibited by mechanical stimulation of the TCCO, or electrical stimulation of its nerve. 6. Octopamine had selective effects on individual remotor units. First, assistance group remotor motor neurons were affected in two ways. One unit was inhibited, so that reflex spiking in response to TCMRO stimulation was abolished. A second unit was not inhibited, but its reflex response mode changed, so that instead of responding to TCMRO input with an assistance reflex, it responded to TCCO input with a resistance reflex. Second, among motor neurons that normally respond to TCCO input with resistance reflexes, these responses were enhanced by octopamine. 7. Promotor motor neurons were inhibited by octopamine and reflex responses were also affected selectively. Responses to TCCO input (assistance reflexes) were abolished; whereas, responses to TCMRO input (resistance reflexes) were relatively less affected. 8. Intracellular recordings revealed that the majority of remotor motor neurons depolarized in the presence of octopamine. In preparations where these could be classified on the basis of TCMRO/ TCCO inputs, all were identified as group 2 (resistance group). A minority of remotor motor neurons were hyperpolarized by octopamine. All of these were identified as group 1 (assistance group), with strong TCMRO input. 9. The majority of promotor motor neurons were depolarized by octopamine. This depolarization was nevertheless inhibitory since it reversed slightly positive to rest and was associated with a substantial fall in inp