Differential effects of cAMP and serotonin on membrane current, action-potential duration, and excitability in somata of pleural sensory neurons of Aplysia

Baxter, Douglas A.; Byrne, John H.

doi:10.1152/jn.1990.64.3.978

Cited by 100 publications

(98 citation statements)

References 41 publications

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“…The finding that sensory neuron excitability is also enhanced with paired training (Fig. 11) suggests that the broadening effect is due to CAMP-dependent closure of S-type K+ channels (Klein et al, 1986;Baxter and Byrne, 1990). While both the excitability and spike-width effects in isolated sensory neurons appear to decay somewhat faster than the synaptic facilitation, the decay is probably accelerated by the frequent posttesting and the long depolarizing test commands (to measure excitability) or action potential trains (to measure spike width) used in these experiments.…”

Section: Discussionmentioning

confidence: 94%

“…Sensory neurons normally exhibit strong spike accommodation during a long depolarizing step command. By itself, 5-HT has a robust anti-accommodationeffect (Klein et al, 1986) which appears to be a purely CAMP-mediated phenomenon as well as a selective assay of the S-type K current (Klein et al, 1986;Baxter and Byrne, 1990;Hochner and Kandel, 1992).…”

Section: Pairing -Specific Facilitation In H7mentioning

confidence: 99%

“…The most extensively studied of these is 5-HT, which facilitates release from sensory neurons by two different processes. The first involves closure of K+ channels, which broadens the presynaptic action potential, increasing Ca2+ influx at transmitter release sites (Klein et al, 1982;Siegelbaum et al, 1982;Baxter and Byrne, 1990;Hochner and Kandel, 1992;Eliot et al, 1993). This effect is mediated in part by CAMP-dependent protein kinase (Castellucci et al, 1982;Shuster et al, 1985;Goldsmith and Abrams, 1992).…”

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Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture

et al. 1994

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Synapses made by Aplysia sensory neurons onto motor- and interneuron followers in the intact nervous system exhibit an associative form of synaptic facilitation that is thought to contribute to classical conditioning of the animal's gill and siphon withdrawal reflex (Hawkins et al., 1983; Walters and Byrne, 1983). Here we demonstrate that a similar associative facilitation can be induced between individual sensory and motor neurons isolated in culture. Pairing tetanic stimulation with either of two facilitatory transmitters, 5-HT or small cardioactive peptide, considerably prolongs facilitation compared to either tetanus or transmitter alone. When corrected for the depression that occurs simply in response to low-frequency testing, the facilitation produced by one pairing trial does not decay for more than 20 min after training. This facilitation requires the temporal pairing (0.5 sec forward interstimulus interval) of the two stimuli, tetanus and 5-HT. Delivering the same two stimuli in an unpaired fashion (1 min forward interval) fails to produce the long-lasting effect. Measurements of spontaneous transmitter release during either paired or unpaired training reveal no changes in unitary mEPSP or mEPSC (“mini”) amplitude, indicating that the facilitation involves a presynaptic mechanism. While both forms of training dramatically increase the initial frequency of spontaneous release, mini frequency does not remain elevated as long as the evoked EPSP following paired training, nor does paired training specifically enhance spontaneous release frequency. Pairing-specific facilitation was not blocked by the protein kinase C inhibitor H7. In contrast, the same training procedure produced pairing-specific increases of sensory neuron excitability and action potential width, suggesting that cAMP-mediated processes are involved in the paired effect. Although Ca2+ influx is necessary for the associative effect (Abrams, 1985), we find that the facilitation does not require influx through L-type voltage-gated Ca2+ channels, since the effect was not blocked by the dihydropyridine antagonist nitrendipine. Together, these findings indicate that the mechanism underlying associative, activity-dependent facilitation is intrinsic to the sensory neuron synapse, that it is presynaptically mediated by processes unique to evoked synaptic transmission, and that it appears to involve a pairing-specific broadening of the presynaptic action potential, allowing enhanced Ca2+ influx through the dihydropyridine- insensitive channels responsible for release.

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Section: Discussionmentioning

confidence: 94%

Section: Pairing -Specific Facilitation In H7mentioning

confidence: 99%

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confidence: 99%

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Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture

et al. 1994

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“…This effect contributes to the increase in membrane excitability and spike broadening following 5-HT application (Klein et al 1982;Pollock et al 1985;Baxter and Byrne 1989). Voltage-dependent K + channels (K v ) can also be phosphorylated by both PKA and PKC, and seem to be involved specifically in spike broadening Byrne 1989, 1990;Goldsmith and Abrams 1992;Sugita et al 1992). Spike broadening is an important mechanism for enhancing synaptic transmission through increased Ca 2+ influx in nerve terminals.…”

Section: Biochemical Pathways Activated By 5-ht In Snsmentioning

confidence: 99%

Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes

Barbas¹,

DesGroseillers²,

Castellucci³

et al. 2003

Learn. Mem.

105

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The neurotransmitter serotonin (5-HT) plays an important role in memory encoding in Aplysia. Early evidence showed that during sensitization, 5-HT activates a cyclic AMP-protein kinase A (cAMP-PKA)-dependent pathway within specific sensory neurons (SNs), which increases their excitability and facilitates synaptic transmission onto their follower motor neurons (MNs). However, recent data suggest that serotonergic modulation during sensitization is more complex and diverse. The neuronal circuits mediating defensive reflexes contain a number of interneurons that respond to 5-HT in ways opposite to those of the SNs, showing a decrease in excitability and/or synaptic depression. Moreover, in addition to acting through a cAMP-PKA pathway within SNs, 5-HT is also capable of activating a variety of other protein kinases such as protein kinase C, extracellular signal-regulated kinases, and tyrosine kinases. This diversity of 5-HT responses during sensitization suggests the presence of multiple 5-HT receptor subtypes within the Aplysia central nervous system. Four 5-HT receptors have been cloned and characterized to date. Although several others probably remain to be characterized in molecular terms, especially the Gs-coupled 5-HT receptor capable of activating cAMP-PKA pathways, the multiplicity of serotonergic mechanisms recruited into action during learning in Aplysia can now be addressed from a molecular point of view.The marine mollusk Aplysia has proven to be a powerful model system for the study of learning and memory. This animal displays several simple forms of nonassociative learning, such as habituation, dishabituation, and sensitization (Pinsker et al. 1970(Pinsker et al. , 1973Carew et al. 1971), but also more complex forms of associative learning such as classical, operant, and fear conditioning (Carew et al. , 1983Walters et al. 1981; Lechner et al. 2000a,b;Brembs et al. 2002). The strength of this model system arises from the relative simplicity of its central nervous system (CNS), which contains a small number of neurons, some of which are well characterized both morphologically and electrophysiologically. Thus, one can study a specific synaptic connection in different animals subjected to a wide variety of behavioral training protocols. For this reason, it has been possible to discover many of the mechanisms of learning and memory in this animal at the behavioral, cellular, and molecular levels, and provide direct evidence that certain forms of learning rely on the plasticity of individual synaptic connections (for review, see Kandel 2001).One of the best characterized forms of learning in Aplysia is sensitization, in which a noxious stimulus facilitates an animal's pre-existing response to the presentation of another innocuous stimulus. It has been most thoroughly studied in the defensive reflex responses of Aplysia. For example, a mild tactile stimulus applied to the tail evokes the retraction of respiratory organs (gill and siphon) inside the mantle cavity situated on the back of the animal. The stre...

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“…In particular, sensitizing stimuli act to enhance both sensory neuron excitability and transmitter release (for review, see Byrne et al 1993;Hawkins et al 1993). These changes occur via the activation of second messenger systems in a time-and state-dependent manner (Baxter and Byrne 1990;Braha et al 1990;Ghirardi et al 1992;Pieroni and Byrne 1992;Sugita et al 1992Sugita et al , 1994Byrne and Kandel 1996). Several of these storage processes operate in parallel to maintain both the short-and long-term components of the memory for sensitization (Frost et al 1985;Greenberg et al 1987;Schwartz and Greenberg 1987;Scholz and Byrne 1988;Bailey et al 1992;Kennedy et al 1992;Byrne et al 1993;Alberini et al 1994;O'Leary et al 1995).…”

Section: Introductionmentioning

confidence: 99%

Role of interneurons in defensive withdrawal reflexes in Aplysia.

Cleary¹,

Byrne²,

Frost³

1995

Learning & Memory

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Differential effects of cAMP and serotonin on membrane current, action-potential duration, and excitability in somata of pleural sensory neurons of Aplysia

Cited by 100 publications

References 41 publications

Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture

Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell culture

Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes

Role of interneurons in defensive withdrawal reflexes in Aplysia.

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