The effect of superfused serotonin (5-HT; 50 microns) on the synaptic responses of the lateral giant (LG) interneuron in crayfish was found to depend on the social status of the animal. In socially isolated animals. 5-HT persistently increased the response of LG to sensory nerve shock. After social isolates were paired in a small cage, they fought and determined their dominant and subordinate status. After 12 d of pairing, 5-HT reversibly inhibited the response of LG in the social subordinate and reversibly increased the response of LG in the social dominant crayfish. The effect of 5-HT changed approximately linearly from response enhancement to inhibition in the new subordinate over the 12 d of pairing. If, after 12 d pairing, the subordinate was reisolated for 8 d, the response enhancement was restored. If the subordinate, instead, was paired with another subordinate and became dominant in this new pair, the inhibitory effect of 5-HT changed to an enhancing effect over the next 12 d of pairing. If, however, two dominant crayfish were paired and one became subordinate, the enhancing effect of 5-HT persisted in the new subordinate even after 38 d pairing. These different effects of serotonin result from the action of two or more molecular receptors for serotonin. A vertebrate 5-HT, agonist had no effect on social isolates but reversibly inhibited the response of LG in both dominant and subordinate crayfish. The inhibitory effects of the agonist developed approximately linearly over the first 12 d of pairing. A vertebrate 5-HT2 agonist persistently increased the response of LG in isolate crayfish and reversibly increased the response of the cell in dominant and subordinate crayfish. Finally, although neurons that might mediate these effects of superfused 5-HT are unknown, one pair of 5-HT-immunoreactive neurons appears to contact the LG axon and initial axon segment in each abdominal ganglion in its projection caudally from the thorax.

Neuromodulation provides a means of changing the excitability of neurons or the effect of synapses, and so extends the performance range of neural circuits. Metamodulation occurs when the neuromodulatory effect is itself modulated, often in response to a change in the behavioral state of the animal. The well-studied neural circuit that mediates escape in the crayfish is modulated by serotonin, and this modulation is subject to two forms of metamodulation. First, the serotonergic modulation of the Lateral Giant (LG) command neuron for escape depends on the pattern of exposure of the cell to serotonin. High and low concentrations, and rapid and slow exposures each produce opposite modulatory effects on sensory-evoked EPSPs in LG. In addition, brief exposures produce transient modulatory effects, whereas longer exposures produce long-term facilitation. These different patterns of exposure may result from serotonin neurotransmission, paracrine transmission, and hormonal release, all of which occur in the vicinity of LG. The second form of metamodulation enables serotonergic modulation to track slow changes in the social status of the crayfish. Slowly applied serotonin facilitates LG’s response in socially isolated crayfish and in new dominant and subordinate animals. Facilitation is retained in the dominant animal during two weeks of continuous pairing of the animals, but facilitation gradually changes to inhibition in the subordinate crayfish. These and related changes in serotonin modulation appear to result from changes in the population of serotonin receptors that mediate the modulatory effects in LG. Whereas the exposure-dependent metamodulation enables rapid changes in serotonergic modulation of LG to occur, the status-dependent metamodulation enables serotonergic modulation of LG to track the slow maturation of social relationships.

The crayfish hindgut is a morphologically differentiated tube that varies along its length in the distribution of muscles and glands, contractile properties, serotonergic innervation, patterns of 5-HT receptor expression, and sensitivity to serotonin (5-HT). Anatomical differences divide the hindgut into five distinct segments along its length. Spontaneous pulsatile contractions produced by the isolated hindgut decrease in force and increase in frequency along the anterior-posterior axis. Central input to the hindgut comes from a large cluster of 5-HT-immunoreactive neurons in the terminal abdominal ganglion that form a large nerve plexus on the hindgut. 5-HT(1alpha) and 5-HT(2beta) receptors vary in their distribution along the hindgut, and are associated with longitudinal and circular muscles and with axon collaterals of the 5-HT-immunoreactive neurons. Application of 30 nmol l(-1) to 1 mumol l(-1) 5-HT to rostral, middle, or caudal sections of hindgut produced tension changes that varied with the concentration and section. 5-HT also initiated antiperistaltic waves in the posterior hindgut. These results indicate that 5-HT is an important neuromodulator for initiating contractions and coordinating activity in the different functional compartments along the rostral-to-caudal axis of the hindgut.

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