Involvement of Presynaptic and Postsynaptic Mechanisms in a Cellular Analog of Classical Conditioning at<i>Aplysia</i>Sensory-Motor Neuron Synapses in Isolated Cell Culture

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

doi:10.1523/jneurosci.18-01-00458.1998

Cited by 101 publications

(91 citation statements)

References 34 publications

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“…They randomly summate during the down state of slow oscillations and may act in concert with slow hyperpolarization-activated cation currents to depolarize cortical pyramidal cells above threshold (49). Assuming that the probability of miniature excitatory postsynaptic potentials during the silent down phase is selectively enhanced at synapses previously activated during associative learning (50)(51)(52)(53), this ongoing miniature activity could well explain the present observation of increased coherence of slow oscillations between cortical regions previously engaged in the learning process.…”

Section: Discussionmentioning

confidence: 60%

Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations

Mölle

Marshall²,

Gais³

et al. 2004

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

189

127

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Learning is assumed to induce specific changes in neuronal activity during sleep that serve the consolidation of newly acquired memories. To specify such changes, we measured electroencephalographic (EEG) coherence during performance on a declarative learning task (word pair associations) and subsequent sleep. Compared with a nonlearning control condition, learning performance was accompanied with a strong increase in coherence in several EEG frequency bands. During subsequent non-rapid eye movement sleep, coherence only marginally increased in a global analysis of EEG recordings. However, a striking and robust increase in learning-dependent coherence was found when analyses were performed time-locked to the occurrence of slow oscillations (<1 Hz). Specifically, the surface-positive half-waves of the slow oscillation resulting from widespread cortical depolarization were associated with distinctly enhanced coherence after learning in the slow-oscillatory, delta, slow-spindle, and gamma bands. The findings identify the depolarizing phase of the slow oscillations in humans as a time period particularly relevant for a reprocessing of memories in sleep.

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Section: Discussionmentioning

confidence: 60%

Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations

Mölle

Marshall²,

Gais³

et al. 2004

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

189

127

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“…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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“…Long-term potentiation (LTP) (Lin & Glanzman, 1994b), as well as several associative forms of learning-related plasticity (Murphy & Glanzman, 1996;Schacher et al 1997;Bao et al 1998), of sensorimotor connections all require a rise in postsynaptic intracellular Ca 2+ . To test whether the effect of 5-HT on the Glu-PSP depends upon intracellular Ca 2+ in the motor neuron, we added BAPTA (100-200 mM) to the standard micropipette solution.…”

Section: Bapta Blocks 5-ht-induced Facilitation Of the Glutamate Respmentioning

confidence: 99%

“…This idea is supported by the discovery that the firing of identified serotonergic facilitatory neurons in Aplysia can remain significantly elevated for > 10 min after a single, brief tail shock . A possible objection to the idea that postsynaptic facilitation contributes to behavioural sensitization comes from a study by Bao et al (1998), who reported that the facilitation of sensorimotor synapses in culture induced by brief treatment with 5-HT is not affected by postsynaptic application of BAPTA. However, we have found that the facilitation of the sensorimotor synapse induced by a 10 min application of 5-HT, or by tail nerve shock, is significantly reduced when BAPTA is present in the motor neuron (Li et al 2001;Roberts & Glanzman, 2001).…”

Section: -Ht Facilitatesmentioning

confidence: 99%

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

Chitwood

Glanzman

2001

The Journal of Physiology

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1. Serotonin (5-HT) facilitates the connections between sensory and motor neurons in Aplysia during behavioural sensitization. The effect of 5-HT on sensorimotor synapses is believed to be primarily presynaptic. Here we tested whether 5-HT can have an exclusively postsynaptic facilitatory effect.2. Siphon motor neurons were individually dissociated from the abdominal ganglion of Aplysia and placed into cell culture. Brief pulses of glutamate, the putative sensory neuron transmitter, were focally applied (0.1 Hz) to solitary motor neurons in culture, and the glutamate-evoked postsynaptic potentials (Glu-PSPs) were recorded.3. When 5-HT was perfused over the motor neuron for 10 min, the amplitude of the Glu-PSPs was significantly increased. The 5-HT-induced enhancement of the Glu-PSPs persisted for at least 40 min after washout.4. Prior injection into the motor neuron of the calcium chelator BAPTA, GDP-b-S or GTP-y-S blocked the 5-HT-induced facilitation of the Glu-PSPs. However, the facilitation was not blocked when APV, an NMDA receptor antagonist, was applied together with the 5-HT.5. The enhancement of the Glu-PSPs by 5-HT was reversed by the AMPA receptor antagonist DNQX, indicating that 5-HT increased the functional expression of AMPA-type receptors in the motor neuron.6. The presence of botulinum toxin in the motor neuron blocked the 5-HT-induced enhancement of the Glu-PSPs. As botulinum toxin prevents exocytosis we hypothesize that during sensitization 5-HT causes the insertion of additional AMPA-type receptors into the postsynaptic membrane of sensorimotor synapses via exocytosis. This postsynaptic mechanism may contribute to facilitation of the synapses.

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Involvement of Presynaptic and Postsynaptic Mechanisms in a Cellular Analog of Classical Conditioning atAplysiaSensory-Motor Neuron Synapses in Isolated Cell Culture

Cited by 101 publications

References 34 publications

Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations

Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations

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

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

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