Serotonin facilitates AMPA‐type responses in isolated siphon motor neurons of <i>Aplysia</i> in culture

Chitwood, Raymond A.; Li, Quan; Glanzman, David L.

doi:10.1111/j.1469-7793.2001.00501.x

Cited by 79 publications

(88 citation statements)

References 27 publications

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“…Postsynaptic injections of gelonin directly into the MN blocked this form of LTF. Reports (30) have described long-term postsynaptic effects of 5-HT at Aplysia SN-MN synapses; 24 h after repeated 5-HT, MNs have an increased depolarizing response to glutamate, which has been hypothesized to be due to an increase in ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor insertion (44). The present study identifies a requirement for postsynaptic protein synthesis in the induction of LTF.…”

Section: Discussionmentioning

confidence: 57%

Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation inAplysia

Sherff

Carew²

2004

Proc. Natl. Acad. Sci. U.S.A.

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The induction of different phases of memory depends on the amount and patterning of training, raising the question of whether specific training patterns engage different cellular mechanisms and whether these mechanisms operate in series or in parallel. We examined these questions by using a cellular model of memory formation: facilitation of the tail sensory neuron-motor neuron synapses by serotonin (5-hydroxytryptamine, 5-HT) in the CNS of Aplysia. We studied facilitation in two temporal domains: intermediate-term facilitation (1.5-3 h) and long-term facilitation (LTF, >24 h). Both forms can be induced by using several different temporal and spatial patterns of 5-HT, including (i) repeated, temporally spaced pulses of 5-HT to both the sensory neuron soma and the sensory neuron-motor neuron synapse, and (ii) temporally asymmetric exposure of 5-HT to the soma and synapse under conditions in which neither exposure alone induces LTF. We first examined the protein and RNA synthesis requirements for LTF induced by these two patterns and found that asymmetric (but not repeated) 5-HT application induced LTF that required postsynaptic protein and RNA synthesis. We next focused on the patterning and protein synthesis requirements for intermediate-term facilitation. We found that intermediate-term facilitation (i) is induced locally at the synapse, (ii) requires multiple pulses of 5-HT, and (iii) requires synaptic protein synthesis. Our findings show that different temporal and spatial patterns of 5-HT induce specific temporal phases of long-lasting facilitation in parallel by engaging different cellular and molecular mechanisms. I t has long been appreciated that memories can persist in dramatically different time frames, from seconds and minutes up to a lifetime (1, 2). A major question now concerns the relationship between memories that exist in different temporal domains. One possibility, for which there is considerable empirical support (see ref. 1), is that memories are processed in series. However, there is a growing body of evidence showing that, at least under certain circumstances, memories can also be processed in parallel (3-7).Like memory, neuronal plasticity can exist in several temporal domains. This feature of plasticity has been revealed in many experimental contexts, including three model systems that have been especially useful for studying the synaptic basis for learning and memory: the mammalian hippocampus (8-11), the photoreceptor neurons in Hermissenda (12, 13), and the sensory neuron-motor neuron (SN-MN) synapses of Aplysia. In Aplysia, the tail-elicited siphon-withdrawal reflex has been useful for examining the temporal relationships between synaptic plasticity and memory. Memory for sensitization induced by repeated tail shocks can exist in at least three temporal domains: short-term memory (Ͻ25 min), intermediate-term memory (Ϸ90 min), and long-term memory (Ͼ24 h) (14-16). Because tail shock releases serotonin (5-hydroxytryptamine, 5-HT) systemically (17) On the synaptic level, ITF exists in m...

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Section: Discussionmentioning

confidence: 57%

Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation inAplysia

Sherff

Carew²

2004

Proc. Natl. Acad. Sci. U.S.A.

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“…The LE membrane property-independent process of facilitation was originally thought to be attributable to presynaptic vesicle mobilization (Gingrich and Byrne, 1985), but it might also involve other mechanisms such as changes in postsynaptic receptors (Chitwood et al, 2001;Li et al, 2005) or synaptic growth. The NO donor DEA/NO produced facilitation that was not associated with any change in LE membrane properties, and NO donors similarly produce presynaptic facilitation or inhibition at other Aplysia synapses without affecting presynaptic membrane properties (Mothet et al, 1996a,b).…”

Section: Role Of No In the Le Membrane Property-independent Process Omentioning

confidence: 99%

“…NO contributes to trafficking and membrane insertion of AMPA receptors during LTP in hippocampus (Huang et al, 2005;Wang et al, 2005). Aplysia sensory-motor neuron EPSPs are thought to be glutamatergic (Dale and Kandel, 1993) AMPA-like glutamate receptors may contribute to heterosynaptic facilitation and homosynaptic potentiation at sensorymotor neuron synapses in vitro (Chitwood et al, 2001;Li et al, 2005). To begin to investigate whether glutamate receptor insertion might contribute to the facilitation during conditioning, we injected an LFS motor neuron with the light chain of botulinum toxin type B, which blocks membrane insertion by blocking exocytosis.…”

Section: Injecting An Inhibitor Of Exocytosis Into a Motor Neuron Redmentioning

confidence: 99%

Role of Nitric Oxide in Classical Conditioning of Siphon Withdrawal inAplysia

Antonov

Ha²,

Antonova³

et al. 2007

J. Neurosci.

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Nitric oxide (NO) is thought to be involved in several forms of learning in vivo and synaptic plasticity in vitro, but very little is known about the role of NO during physiological forms of plasticity that occur during learning. We addressed that question in a simplified preparation of the Aplysia siphon-withdrawal reflex. We first used in situ hybridization to show that the identified L29 facilitator neurons express NO synthase. Furthermore, exogenous NO produced facilitation of sensory-motor neuron EPSPs, and an inhibitor of NO synthase or an NO scavenger blocked behavioral conditioning. Application of the scavenger to the ganglion or injection into a sensory neuron blocked facilitation of the EPSP and changes in the sensory-neuron membrane properties during conditioning. Injection of the scavenger into the motor neuron reduced facilitation without affecting sensory neuron membrane properties, and injection of an inhibitor of NO synthase had no effect. Postsynaptic injection of an inhibitor of exocytosis had effects similar to injection of the scavenger. However, changes in the shape of the EPSP during conditioning were not consistent with postsynaptic AMPA-like receptor insertion but were mimicked by presynaptic spike broadening. These results suggest that NO makes an important contribution during conditioning and acts directly in both the sensory and motor neurons to affect different processes of facilitation at the synapses between them. In addition, they suggest that NO does not come from either the sensory or motor neurons but rather comes from another source, perhaps the L29 interneurons.

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“…It involves facilitation of AMPA-type responses to glutamate, the putative neurotransmitter released by SNs, in cultured LFS neurons (Chitwood et al 2001), and could possibly take place during sensitization training.…”

Section: Modulation Of Defensive Reflex Circuits By 5-ht During Sensimentioning

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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Serotonin facilitates AMPA‐type responses in isolated siphon motor neurons of Aplysia in culture

Cited by 79 publications

References 27 publications

Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation inAplysia

Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation inAplysia

Role of Nitric Oxide in Classical Conditioning of Siphon Withdrawal inAplysia

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

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