Summary
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1.
The bilaterally paired ventral white cells (VWCs) of the buccal ganglion ofPleurobranchaea drive rhythmic motor output in the neural network controlling the movements of the buccal mass, which mediates both ingestion and egestion behaviors. The VWCs exert their action during minutes-long episodes of endogenously sustained depolarization and repetitive firing attended by pronounced action potential broadening (Gillette et al. 1980). In isolated preparations the ability to sustain such burst episodes is variable and somewhat labile (Gillette et al. 1980). We have assessed the ability of the intracellular messenger cyclic-3′,5′-adenosine monophosphate (cAMP), its non-hydrolyzable analogs and inhibitors of degradation to stimulate action potential broadening and bursting in the VWC.
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2.
Intracellular injection of cAMP enhances progressive spike broadening (Figs. 1 and 2C) and stimulates spontaneous spiking activity and endogenous burst episodes in an apparent dose-dependent fashion (Fig. 2). Bath application of cAMP analogs or the phosphodiestrase inhibitor isobutylmethylxanthine also stimulates spike broadening and recurrent burst episodes in the intact neuron (Figs. 3 and 5) and induces the capacity to sustain prolonged bursts triggered by brief current stimulation in the isolated neuron cell body (Fig. 4).
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3.
Work described in in the preceding paper (Gillette et al. 1982) suggested that regulation of (Ca++)i may affect progressive spike broadening in the VWC via a Ca++-activated K+ current (IK,Ca) and possibly via inward Ca++ current. The action of cAMP in enhancing spike broadening resembles that of agents and treatments that reduce (Ca++)i and/or suppress IK,Ca. Further, cAMP stimulation reverses a suppres sion of spike broadening caused by high Ca++ saline (Fig. 5) (which may increase [Ca++]i) and, conversely, that intracellular injection of a ‘high’ Ca++ buffer (Ca++-EGTA, 5 × 10−7 free Ca++) reverses the cAMP stimulation of spike broadening (Fig. 6).
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4.
Stimulation with cAMP causes an abbreviation of the waveform and amplitude of the undershoots of single, unbroadened action potentials; this action resembles the effect of agents and treatments that reduce [Ca++]i and/or IK,Ca (Figs. 7, 8). This effect is reversed by intracellular injection of high Ca++ buffer (Fig. 9).
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5.
These results suggest that one possible mechanism of action of cAMP is to reduce the ability or availability of intracellular free Ca++ to activate IK,Ca. A non-exclusive alternative is that cAMP enhances a Ca++ current. The evidence that both of these mechanisms could be regulated by an increase in the internal Ca++ buffering ability of the cell is discussed.
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6.
The potential context of the VWC's behavioral function is one in which their command ability is induced by sensory or other input during arousal of some buccal behavior through neurotransmitter stimulation of endogenous cAMP.
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Abbreviations
- cAMP :
-
cyclic-3′,5′-adenosine monophosphate
- IBMX :
-
isobutylmethylxanthine
- CPT-cAMP :
-
8-p-chlorophenyl-thio-adenosine-3′,5′-cyclic monophosphoric acid
- VWC :
-
ventral white cell
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Gillette, R., Gillette, M.U. & Davis, W.J. Substrates of command ability in a buccal neuron ofPleurobranchaea . J. Comp. Physiol. 146, 461–470 (1982). https://doi.org/10.1007/BF00609442
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DOI: https://doi.org/10.1007/BF00609442