Serotonin Transduction Cascades Mediate Variable Changes in Pyloric Network Cycle Frequency in Response to the Same Modulatory Challenge

Abstract

Serotonin transduction cascades mediate variable changes in pyloric network cycle frequency in response to the same modulatory challenge. J Neurophysiol 99: 2844 -2863. First published April 9, 2008 doi:10.1152/jn.00986.2007. A fundamental question in systems biology addresses the issue of how flexibility is built into modulatory networks such that they can produce context-dependent responses. Here we examine flexibility in the serotonin (5-HT) response system that modulates the cycle frequency (cf) of a rhythmic motor output. We found that depending on the preparation, the same 5-min bath application of 5-HT to the pyloric network of the California spiny lobster, Panulirus interruptus, could produce a significant increase, decrease, or no change in steady-state cf relative to baseline. Interestingly, the mean circuit output was not significantly different among preparations prior to 5-HT application. We developed pharmacological tools to examine the preparation-to-preparation variability in the components of the 5-HT response system. We found that the 5-HT response system consisted of at least three separable components: a 5-HT 2␤Pan -like component mediated a rapid decrease followed by a sustained increase in cf; a 5-HT 1␣Pan -like component produced a small and usually gradual increase in cf; at least one other component associated with an unknown receptor mediated a sustained decrease in cf. The magnitude of the change in cf produced by each component was highly variable, so that when summed they could produce either a net increase, decrease, or no change in cf depending on the preparation. Overall, our research demonstrates that the balance of opposing components of the 5-HT response system determines the direction and magnitude of 5-HT-induced change in steady-state cf relative to baseline.

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).…”

Consequences of acute and long-term removal of neuromodulatory input on the episodic gastric rhythm of the crabCancer borealis

“…5B). How this variability arises in network output is unclear, although many sources of variability have been identified in the STG that could contribute to these observations, including variable ion channel expression (Schulz et al 2006(Schulz et al , 2007, synaptic strength (Goaillard et al 2009;Johnson et al 1991;Thirumalai et al 2006), and response to neuromodulation (Nusbaum and Marder 1989b;Spitzer et al 2008). Decentralization increased the across-preparation variability of relative phase relationships between LG and DG neurons but did ig.…”

D1-like dopamine receptors downregulate Na+-K+-ATPase activity and increase cAMP production in the posterior gills of the blue crabCallinectes sapidus

“…There are studies showing that D 1 -like receptor drugs, such as fenoldopam and SCH23390, have high affinities for serotonin receptors (12,35), a possibility with the high concentrations (10 M) used in previous reports. Several crustacean serotonin receptors, which also increase cAMP production upon stimulation, have been reported in the somatogastric ganglion but not in the gills; these crustacean serotonin receptors are not pharmacologically similar to vertebrate serotonin receptors (14,46,47). Octopamine (OA), a biogenic monoamine structurally related to norepinephrine, acts as a neurohormone, neuromodulator, and neurotransmitter in invertebrates, including the crustaceans.…”