Metamodulation of the Crayfish Escape Circuit

Abstract

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 Activity of Isolated Neurons and the Modulatory State of an Isolated Nervous System Represent a Recent Behavioural State

“…Recent reports demonstrating that behavioural state induced changes in receptor gene expression (Whitaker et al, 2011), neuronal response to neurotransmitters (Yeh et al, 1996;Edwards et al, 2002) and in neurotransmitter synthesis (Hatcher et al, 2008) at the single-cell level are in line with this point of view as well.…”

Neural Circuit Reconfiguration by Social Status

“…Whatever signals produce the modulatory changes associated with social status can be seen to affect serotonergic modulation of neuronal circuits, as well as the circuits themselves. This metamodulation, which is also seen in the effect of status on serotonergic modulation of escape (Edwards et al, 2002), is a general phenomenon (Katz and Edwards, 1999) that affects the behavioral states and hormonal function in a variety of animals (Fernald, 2002;Robinson et al, 2008;O'Connell and Hofmann, 2011).…”

Variability, compensation, and modulation in neurons and circuits

“…Responses of individual neurons, synapses, and circuits to neuromodulation are often quite variable (50,51). In some instances, it is clear that the effect of the modulator depends on some obvious feature of the state of the preparation (52)(53)(54)(55)(56). In some instances, this variability arises from unknown sources and is likely a consequence of differing underlying cell or circuit parameters.…”