Involvement of Pre- and Postsynaptic Mechanisms in Posttetanic Potentiation at
            <i>Aplysia</i>
            Synapses

Bao, Jianxin; Kandel, Eric R.; Hawkins, Robert D.

doi:10.1126/science.275.5302.969

Cited by 105 publications

(105 citation statements)

References 28 publications

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“…7-9). The amount of recovery in our experiments is comparable to that reported by others both in intact ganglia (Walters and Byrne, 1985;Trudeau and C astellucci, 1992;Nakanishi et al, 1997) and in conventional cultures using extracellular stimulation (Lin and Glanzman, 1994;Bao et al, 1997). Five to 10 minutes after one stimulus, the EPSP in the cultures averaged 0.78 of the initial EPSP, after three stimuli it was 0.63, and after 8 -10 stimuli it was 0.47.…”

Section: Studies Of Depression and Facilitation At Aplysia Sensorimotsupporting

confidence: 77%

Switching Off and On of Synaptic Sites atAplysiaSensorimotor Synapses

2000

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Using the highly plastic synapses between mechanoreceptor sensory neurons and siphon motor neurons of Aplysia as a model, we have investigated whether switching off and on of individual synaptic release sites is a strategy that is used by neurons in forms of short-term synaptic modulation with a time course of minutes to hours. We have modified some of the techniques of classical quantal analysis and examined the kinetics of synaptic depression under different stimulation protocols to answer this question. Our analysis shows that both synaptic depression caused by homosynaptic activity and synaptic facilitation induced by an endogenous facilitatory transmitter occur by means of the shutting off and turning on, respectively, of synaptic sites, without intermediate changes in the probability of release. Our findings imply that other forms of plasticity at these synapses, such as post-tetanic potentiation, long-term facilitation, and long-term potentiation, are also expressed by all-or-none changes in activity at individual sites. We thus show that in addition to the mechanisms of synaptic integration that are known to operate in single cells and networks, neurons can exercise a further layer of fine control, at the level of individual release sites.Key words: synaptic transmission; synaptic plasticity; synaptic depression; synaptic facilitation; transmitter release; quantal analysis; miniature synaptic potentials Synaptic phenomena such as long-term potentiation and depression represent cellular mechanisms that may contribute to learning (McKernan and Shinnick-Gallagher, 1997;Murphy and Glanzman, 1997;Rogan et al., 1997), as do short-term processes such as homosynaptic depression and heterosynaptic facilitation (Zucker, 1972;Byrne et al., 1993;Cohen et al., 1997). Although detailed mechanistic explanations for these phenomena are lacking, evidence has been marshalled for such general possibilities as changes in the probability of neurotransmitter release (Bolshakov and Siegelbaum, 1994;Stevens and Wang, 1994) or the insertion or activation of postsynaptic receptors (Isaac et al., 1995;Liao et al., 1995). Other studies have reported that some synapses release no neurotransmitter initially but can be recruited by various treatments (Wojtowicz et al., 1991;Charpier et al., 1995;Wang et al., 1996). We have taken advantage of the favorable properties of sensorimotor synapses of Apl ysia to examine whether shifting of synapses into and out of the active pool occurs in short-term synaptic plasticity.Modulation of sensorimotor transmission in Apl ysia contributes to changes in its responsiveness to tactile stimulation (Carew et al., 1983;Byrne et al., 1993;Stopfer and C arew, 1996;Cohen et al., 1997). Homosynaptic depression is a progressive decline in transmitter release that occurs even at low stimulation frequency (C astellucci and Kandel, 1974). Heterosynaptic facilitation is the increase in transmitter release, mediated by facilitatory transmitters such as serotonin (5HT), that follows a noxious stimulus (Brunelli e...

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Section: Studies Of Depression and Facilitation At Aplysia Sensorimotsupporting

confidence: 77%

Switching Off and On of Synaptic Sites atAplysiaSensorimotor Synapses

2000

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“…Our results provide evidence for a direct link between HCN current and learning in the semiintact siphon withdrawal preparation of Aplysia. In this case the role of HCN current appears to be similar to its role during LTP at Schaffer collateral-CA1 synapses in hippocampus (23), presenting an interesting example of convergent evolution in memory circuits: HCN enhances NMDA receptor current required for Hebbian potentiation, which contributes to classical conditioning of the withdrawal reflex in Aplysia (29,(52)(53)(54)(55). In neither preparation is it known how HCN current enhances NMDA current, but it might act either by depolarizing the postsynaptic neuron or by a receptor-receptor interaction.…”

Section: Discussionmentioning

confidence: 99%

“…4 A and B) in which the reflex is mediated in part by monosynaptic excitatory postsynaptic potentials (EPSPs) from LE siphon sensory neurons to LFS siphon motor neurons in the abdominal ganglion (30). Sensitization is due in part to presynaptic facilitation of those EPSPs by PKA (43,44) and conditioning to activity-dependent facilitation of the EPSPs (28), which involves two mechanisms that interact (29): activity-dependent enhancement of the facilitation due to Ca 2+ priming of adenylyl cyclase and greater production of cAMP and activation of PKA in the sensory neurons (43)(44)(45)(46)(47)(48)(49)(50)(51), and Hebbian potentiation due to Ca 2+ influx through NMDA-like receptor channels in the motor neurons (52)(53)(54)(55).…”

Section: Hcn Channels Contribute To Behavioral Conditioning But Notmentioning

confidence: 99%

Hyperpolarization-activated, cyclic nucleotide-gated cation channels in Aplysia : Contribution to classical conditioning

Yang

Kuzyk

Antonov

et al. 2015

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

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Hyperpolarization-activated, cyclic nucleotide-gated cation (HCN) channels are critical regulators of neuronal excitability, but less is known about their possible roles in synaptic plasticity and memory circuits. Here, we characterized the HCN gene organization, channel properties, distribution, and involvement in associative and nonassociative forms of learning in Aplysia californica. Aplysia has only one HCN gene, which codes for a channel that has many similarities to the mammalian HCN channel. The cloned acHCN gene was expressed in Xenopus oocytes, which displayed a hyperpolarization-induced inward current that was enhanced by cGMP as well as cAMP. Similarly to its homologs in other animals, acHCN is permeable to K + and Na + ions, and is selectively blocked by Cs + and ZD7288. We found that acHCN is predominantly expressed in inter-and motor neurons, including LFS siphon motor neurons, and therefore tested whether HCN channels are involved in simple forms of learning of the siphon-withdrawal reflex in a semiintact preparation. ZD7288 (100 μM) significantly reduced an associative form of learning (classical conditioning) but had no effect on two nonassociative forms of learning (intermediate-term sensitization and unpaired training) or baseline responses. The HCN current is enhanced by nitric oxide (NO), which may explain the postsynaptic role of NO during conditioning. HCN current in turn enhances the NMDA-like current in the motor neurons, suggesting that HCN channels contribute to conditioning through this pathway.HCN channels | learning and memory | NMDA | nitric oxide | Aplysia H yperpolarization-activated, cyclic nucleotide-gated (HCN), cation nonselective ion channels generate hyperpolarization-activated inward currents (I h ) and thus tend to stabilize membrane potential (1-3). In addition, binding of cyclic nucleotides (cAMP and cGMP) to the C-terminal cyclic nucleotide binding domain (CNBD) enhances I h and thus couples membrane excitability with intracellular signaling pathways (2, 4). HCN channels are widely important for numerous systemic functions such as hormonal regulation, heart contractility, epilepsy, pain, central pattern generation, sensory perception (4-15), and learning and memory (16-24).However, in previous studies it has been difficult to relate the cellular effects of HCN channels directly to their behavioral effects, because of the immense complexity of the mammalian brain. We have therefore investigated the role of HCN channels in Aplysia, which has a numerically simpler nervous system (25). We first identified and characterized an HCN gene in Aplysia, and showed that it codes for a channel that has many similarities to the mammalian HCN channel. We found that the Aplysia HCN channel is predominantly expressed in motor neurons including LFS neurons in the siphon withdrawal reflex circuit (26, 27). We therefore investigated simple forms of learning of that reflex in a semiintact preparation (28-30) and found that HCN current is involved in classical conditioning and enhances the ...

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“…Cell culture and electrophysiological methods were generally the same as described previously (23,(63)(64)(65) (SI Materials and Methods). Cocultures consisting of an L7 gill motor neuron and one or two pleural sensory neurons were used 4-6 d after plating.…”

Section: Methodsmentioning

confidence: 99%

Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation inAplysia

Jin

Puthanveettil

Udo

et al. 2012

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

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Long-term plasticity can differ from short-term in recruiting the growth of new synaptic connections, a process that requires the participation of both the presynaptic and postsynaptic components of the synapse. How does information about synaptic plasticity spread from its site of origin to recruit the other component? The answer to this question is not known in most systems. We have investigated the possible role of spontaneous transmitter release as such a transsynaptic signal. Until recently, relatively little has been known about the functions of spontaneous release. In this paper, we report that spontaneous release is critical for the induction of a learning-related form of synaptic plasticity, long-term facilitation in Aplysia. In addition, we have found that this signaling is engaged quite early, during an intermediate-term stage that is the first stage to involve postsynaptic as well as presynaptic molecular mechanisms. In a companion paper, we show that spontaneous release from the presynaptic neuron acts as an orthograde signal to recruit the postsynaptic mechanisms of intermediate-term facilitation and initiates a cascade that can culminate in synaptic growth with additional stimulation during long-term facilitation. Spontaneous release could make a similar contribution to learning-related synaptic plasticity in mammals.serotonin | cell culture | miniature excitatory postsynaptic current | octopamine | botulinum toxin S pontaneous transmitter release was discovered 60 y ago by Fatt and Katz (1), who found that it represents the quantal unit of transmitter release evoked by a presynaptic action potential. However, until recently, relatively little has been known about other possible functions of spontaneous release. In the last few years, we have learned that spontaneous release can contribute to postsynaptic firing (2, 3), regulation of postsynaptic kinase pathways (4), and maintenance of postsynaptic dendritic spines and receptors (5, 6). Spontaneous release has also been found to contribute to some cases of homeostatic scaling of synaptic strength (7-14). Here we report a role of spontaneous transmitter release in the induction of a learning-related form of synaptic plasticity, longterm facilitation produced by serotonin (5HT) in Aplysia.Long-term plasticity can differ from short-term in recruiting the growth of new synaptic connections, a process that requires the participation of both the presynaptic and postsynaptic components of the synapse (15-21). Because short-term plasticity often involves only one component of the synapse (22-24), the question arises: How does information about synaptic plasticity spread from its site of origin to recruit the other component of the synapse? Studies of synaptic growth during development have revealed a fairly elaborate program of pre-and postsynaptic changes involving a variety of orthograde and retrograde messengers (25), including activity-dependent or spontaneous release of the transmitter itself (26-30). We have now investigated the possible role of spo...

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Involvement of Pre- and Postsynaptic Mechanisms in Posttetanic Potentiation at Aplysia Synapses

Cited by 105 publications

References 28 publications

Switching Off and On of Synaptic Sites atAplysiaSensorimotor Synapses

Switching Off and On of Synaptic Sites atAplysiaSensorimotor Synapses

Hyperpolarization-activated, cyclic nucleotide-gated cation channels in Aplysia : Contribution to classical conditioning

Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation inAplysia

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