Reduction of two voltage-dependent K+ currents mediates retention of a learned association

Alkon, Daniel L.; Sakakibara, Manabu; Forman, Robin R.; Harrigan, June F.; Lederhendler, Izja; Farley, Joseph

doi:10.1016/s0163-1047(85)90296-1

Cited by 161 publications

(100 citation statements)

References 44 publications

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“…The short-and long-term facilitation in Aplysia caused by cAMP cascade required the prolongation of an action potential and a de novo protein synthesis, respectively (Siegelbaum et al, 1982;Sweatt and Kandel, 1989;Hochner and Kandel, 1992;Schacher et al, 1993;O'Leary et al, 1995;Sugita et al, 1997;Abel and Kandel, 1998). Even in the CNS of Hermissenda in which intracellular Ca 2+ plays an important role in the signal transduction (Alkon et al, 1992;Ito et al, 1994), the longlasting depolarization due to a reduction in K + -channel conductance and the increase in specific mRNA were reported in the synaptic enhancement in a classical conditioning (Alkon et al, 1985;Nelson and Alkon, 1990). To gain a deeper insight into the excitability of the presynaptic CGC, the duration of the current-evoked and the spontaneous spikes at 30% and 70% from their bottoms were also examined (see the methods in Klein (1993).…”

Section: Discussionmentioning

confidence: 99%

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

Nakamura¹,

Kobayashi²,

Kojima³

et al. 1999

Zoological Science

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ABSTRACT-The cerebral giant cell (CGC) is known to play a crucial role in the regulation of feeding response in the pond snail, Lymnaea stagnalis. However, the mechanisms of signal transduction from the CGC to the following buccal motor neurons are not clear. In the present study, we examined whether cyclic AMP (cAMP)-dependent protein kinase (PKA) contributes to enhancement of a monosynaptic connection between the presynaptic CGC and the postsynaptic buccal motor neuron 1 (B1 cell). Injection of cAMP into the CGC or inhibition of phosphodiesterase by isobutylmethylxanthine in the CGC increased the amplitude of excitatory postsynaptic potential (EPSP) in the B1 cell, whereas no changes were detected in the electrical properties of the CGC. The synaptic enhancement in the B1 cell was completely blocked by inhibition of PKA in the CGC but did not require a de novo protein synthesis due to a PKA phosphorylation. The increase in the EPSP amplitude of B1 cell was associated with the increase in the amount of serotonin release from the CGC. These results hence provided the physiological evidence of the direct regulation of a synaptic enhancement by PKA in the CNS of L. stagnalis, indicating the completely different mechanism from that in the well-studied siphon-and gill-withdrawal reflex in Aplysia.

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Section: Discussionmentioning

confidence: 99%

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

Nakamura¹,

Kobayashi²,

Kojima³

et al. 1999

Zoological Science

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“…The intrinsic excitability of neurons has a crucial impact on the function of neural networks and is modified during the learning task in a variety of species (Alkon et al, 1985;Cleary et al, 1998;Antonov et al, 2001;Burrell et al, 2001;Aizenman et al, 2003). In contrast to the detailed analysis of synaptic long-term potentiation (LTP), a cellular model for learning and memory (Bliss and Collingridge, 1993;Malenka and Nicoll, 1999;Choi et al, 2000), less attention has been given to activity-dependent changes in the intrinsic excitability of neurons.…”

Section: Introductionmentioning

confidence: 99%

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Kang²,

Jiang³

et al. 2005

J. Neurosci.

159

178

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The efficiency of neural circuits is enhanced not only by increasing synaptic strength but also by increasing intrinsic excitability. In contrast to the detailed analysis of long-term potentiation (LTP), less attention has been given to activity-dependent changes in the intrinsic neuronal excitability. By stimulating hippocampal CA1 pyramidal neurons with synaptic inputs correlating with postsynaptic neuronal spikes, we elicited an LTP of intrinsic excitability (LTP-IE) concurring with synaptic LTP. LTP-IE was manifested as a decrease in the action potential threshold that was attributable to a hyperpolarized shift in the activation curve of voltage-gated sodium channels (VGSCs) rather than activity-dependent changes in synaptic inputs or A-type K ϩ channels. Cell-attached patch recording of VGSC activities indicated such an activity-dependent change in VGSCs. Induction of LTP-IE was blocked by the NMDA receptor antagonist APV, intracellular BAPTA, the CaM kinase inhibitors KN-62 and autocamtide-2-related inhibitory peptide, and the protein synthesis inhibitors emetine and anisomycin. The results suggest that induction of LTP-IE shares a similar signaling pathway with the late phase of synaptic LTP and requires activation of the NMDA glutamate receptor subtype, Ca 2ϩ influx, activity of CaM kinase II, and function of the protein synthesis. This new form of hippocampal neuronal plasticity could be a cellular correlate of learning and memory besides synaptic LTP.

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“…First, it is possible that spike width (and not frequency) increases following conditioning in Herm i s s e n d a . This is unlikely though, given that paired presentations of light and rotation result in a reduction of the fast, transient K + current (IA) and the Ca 2 +-dependent K + current (IK.Ca; Alkon et al 1985), both of which should affect spike frequency to a greater degree than spike width (for a description, see Rogawski 1985). A second possibility is that we simply cannot detect changes in spike frequency in the intact, isolated eyes.…”

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confidence: 99%

Higher-order associative processing in Hermissenda suggests multiple sites of neuronal modulation.

Rogers

Matzel²

1996

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Reduction of two voltage-dependent K+ currents mediates retention of a learned association

Cited by 161 publications

References 44 publications

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

PKA-Dependent Regulation of Synaptic Enhancement between a Buccal Motor Neuron and Its Regulatory Interneuron in Lymnaea stagnalis

Activity-Dependent Long-Term Potentiation of Intrinsic Excitability in Hippocampal CA1 Pyramidal Neurons

Higher-order associative processing in Hermissenda suggests multiple sites of neuronal modulation.

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