Mechanisms of pattern generation underlying swimming in Tritonia. III. Intrinsic and synaptic mechanisms for delayed excitation

Getting, Peter A.

doi:10.1152/jn.1983.49.4.1036

Cited by 146 publications

(108 citation statements)

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“…A diversity of firing patterns in response to constant current injections is a hallmark of neurons in the CNS in many invertebrates and vertebrates (Byrne, 1980;Getting, 1983;Connors and Gutnick, 1990;Kawaguchi, 1995). Similarly, a diverse profile of firing was observed in giant neuron cultures of Drosophila.…”

Section: Classification Of Firing Patterns In Wild-type Neuronsmentioning

confidence: 95%

“…In identified neurons of other species, prepulse protocols have been shown to be an effective means for detecting the presence of a transient, inactivating K ϩ current and assessing its involvement in regulating spiking activities (Byrne, 1980;Getting, 1983). As shown in Figure 3A, spike initiation by current injection was modified differentially by conditioning prepulses in different categories of neurons.…”

Section: Voltage-dependent K ؉ Currents In the Regulation Of Firing Pmentioning

confidence: 99%

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Alterations in Frequency Coding and Activity Dependence of Excitability in Cultured Neurons ofDrosophilaMemory Mutants

Zhao

1997

J. Neurosci.

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Mutants of the Drosophila dunce (dnc) and rutabaga (rut) genes, which encode a cAMP-specific phosphodiesterase and a calcium/calmodulin-responsive adenylyl cyclase, respectively, are deficient in short-term memory. Altered synaptic plasticity has been demonstrated at neuromuscular junctions in these mutants, but little is known about how their central neurons are affected. We examined this problem by using the "giant" neuron culture, which offers a unique opportunity to analyze mutational effects on neuronal activity and the underlying ionic currents in Drosophila. On the basis of instantaneous frequency and first latency of spikes evoked by current steps, four categories of firing patterns (tonic, adaptive, delayed, and interrupted) were identified in wild-type neurons, revealing interesting parallels to those commonly observed in vertebrate CNS neurons. The distinct firing patterns were correlated with expression of different ratios of 4-aminopyridine-and tetraethylammoniumsensitive K ϩ currents. Subsets of dnc and rut neurons displayed abnormal spontaneous spikes and altered firing patterns. Altered frequency coding in mutant neurons was demonstrated further by using stimulation protocols involving conditioning with previous activity. Abnormal spike activity and reduced K ϩ current remained in double-mutant neurons, suggesting that the opposite effects on cAMP metabolism by dnc and rut do not counterbalance the mutual functional defects. The aberrant spontaneous activity and altered frequency coding in different stimulus paradigms may present problems in the stability and reliability of neural circuits for information processing during certain behavioral tasks, raising the possibility of modulation in neuronal excitability as a cellular mechanism underlying learning and memory.

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Section: Classification Of Firing Patterns In Wild-type Neuronsmentioning

confidence: 95%

Section: Voltage-dependent K ؉ Currents In the Regulation Of Firing Pmentioning

confidence: 99%

Alterations in Frequency Coding and Activity Dependence of Excitability in Cultured Neurons ofDrosophilaMemory Mutants

Zhao

1997

J. Neurosci.

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“…Neurons were identified by soma location, coloration, synaptic connectivity, and activity pattern at rest and during the swim motor program as previously described (Getting, 1981(Getting, , 1983. For simplicity, we will refer to VSI-B as VSI for the remainder of this study.…”

Section: Methodsmentioning

confidence: 99%

“…During the swim motor pattern, DSI and VSI fire bursts of action potentials at 8 -20 Hz in an alternating manner with a cycle period of 4 -12 s (Fig. 9Aii) (Getting, 1981(Getting, , 1983. The swim motor pattern terminates after a VSI burst, and then DSI continues to fire tonically at 1-2 Hz, whereas VSI stays silent unless the animal receives tactile stimulation (Popescu and Frost, 2002).…”

Section: Functional Significance Of the Dsi Actionmentioning

confidence: 97%

State-, Timing-, and Pattern-Dependent Neuromodulation of Synaptic Strength by a Serotonergic Interneuron

Sakurai¹,

Katz²

2009

J. Neurosci.

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Here we report that a serotonergic neuron evokes two distinct neuromodulatory actions with different state, timing, and firing pattern dependencies. These neuromodulatory actions may have important behavioral functions. In the mollusc, Tritonia diomedea, EPSCs evoked by ventral swim interneuron B (VSI) exhibited intrinsic plasticity; after a spike train, EPSC amplitude increased from a basal state to a potentiated state, which usually lasted Ͼ10 min. While the synapse was in a potentiated state, stimulation of a serotonergic dorsal swim interneuron (DSI) decreased VSI synaptic strength, returning it to a basal state. The extent of the DSI-evoked decrement was strongly correlated with the magnitude of the homosynaptic potentiation. This synaptic reset, or depotentiation, by DSI was blocked by the serotonin receptor antagonist methysergide and mimicked by a serotonin puff. In contrast to this state-dependent neuromodulatory action, we found that a previously described DSI-evoked transient enhancement of VSI synaptic strength was state-independent, producing the same multiplicative increase in EPSC amplitude regardless of whether the synapse was in a potentiated or basal state. These two actions also differed in their dependencies on the firing pattern of DSI and VSI action potentials. Results suggest that stateindependent synaptic enhancement by DSI may play a short-term role during a swim motor pattern, whereas state-dependent actions may have longer-lasting consequences, resetting VSI synaptic strength after a swim bout. Thus, differences in two neuromodulatory actions at one synapse may allow a serotonergic neuron to play distinct roles at different stages of a motor pattern.

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“…C2 and DSI were identified on the basis of their soma location, appearance, action potential shape, and activity during a swim motor pattern (Getting 1983;Getting et al 1980;Taghert and Willows 1978). Neurons were excluded from the study if they were damaged during the dissection or microelectrode impalement and had resting potentials outside of the normal range of Ϫ40 to Ϫ55 mV.…”

Section: E T H O D Smentioning

confidence: 99%

Transient Enhancement of Spike-Evoked Calcium Signaling by a Serotonergic Interneuron

Hill¹,

Sakurai²,

Katz³

2008

Journal of Neurophysiology

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Hill ES, Sakurai A, Katz PS. Transient enhancement of spikeevoked calcium signaling by a serotonergic interneuron. J Neurophysiol 100: 2919 -2928, 2008. First published September 24, 2008 doi:10.1152/jn.90979.2008. Enhancement of presynaptic Ca 2ϩ signals is widely recognized as a potential mechanism for heterosynaptic potentiation of neurotransmitter release. Here we show that stimulation of a serotonergic interneuron increased spike-evoked Ca 2ϩ in a manner consistent with its neuromodulatory effect on synaptic transmission. In the gastropod mollusk, Tritonia diomedea, stimulation of a serotonergic dorsal swim interneuron (DSI) at physiological rates heterosynaptically enhances the strength of output synapses made by another swim interneuron, C2, onto neurons in the pedal ganglion. Using intracellular electrophysiological recording combined with real-time confocal imaging of C2 (loaded with Oregon Green Bapta 1), it was determined that DSI stimulation increases the amplitude of spike-evoked Ca 2ϩ signals in C2 without altering basal Ca 2ϩ signals. This neuromodulatory action was restricted to distal neurites of C2 where synapses with pedal neurons are located. The effect of DSI stimulation on C2 spike-evoked Ca 2ϩ signals resembled DSI heterosynaptic enhancement of C2 synapses in several measures: both decayed within 15 s, both were abolished by the serotonin receptor antagonist, methysergide, and both were independent of DSI's depolarizing actions on C2. A brief puff of serotonin could mimic the enhancement of spike-evoked Ca 2ϩ signals in the distal neurites of C2, but larger puffs or bath-applied serotonin elicited nonphysiological effects. These results suggest that DSI heterosynaptic enhancement of C2 synaptic strength may be mediated by a local enhancement of spike-evoked Ca 2ϩ signals in the distal neurites of C2.

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Mechanisms of pattern generation underlying swimming in Tritonia. III. Intrinsic and synaptic mechanisms for delayed excitation

Cited by 146 publications

References 0 publications

Alterations in Frequency Coding and Activity Dependence of Excitability in Cultured Neurons ofDrosophilaMemory Mutants

Alterations in Frequency Coding and Activity Dependence of Excitability in Cultured Neurons ofDrosophilaMemory Mutants

State-, Timing-, and Pattern-Dependent Neuromodulation of Synaptic Strength by a Serotonergic Interneuron

Transient Enhancement of Spike-Evoked Calcium Signaling by a Serotonergic Interneuron

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