Non-Associative Learning and Serotonin Induce Similar Bi-Directional Changes in Excitability of a Neuron Critical for Learning in the Medicinal Leech

Burrell, Brian D.; Sahley, Christie L.; Muller, Kenneth J.

doi:10.1523/jneurosci.21-04-01401.2001

Cited by 84 publications

(102 citation statements)

References 61 publications

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“…The correlation of decrease in the AP threshold with learning-related behavior changes has been established by several groups (Schreurs et al, 1997(Schreurs et al, , 1998Burrell et al, 2001). LTP-IE expressed as a hyperpolarized shift in the activation property of VGSCs in this study adds another piece of evidence to support this important concept.…”

Section: Cooperation Of Activity-dependent Intrinsic Plasticitysupporting

confidence: 69%

“…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%

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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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Section: Cooperation Of Activity-dependent Intrinsic Plasticitysupporting

confidence: 69%

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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“…These changes in excitability could be implicated in learning and memory because increases in neuronal excitability are reported in hippocampal and cerebellar neurons after classical conditioning (26,27). In invertebrates, bidirectional changes in excitability are induced concomitantly with sensitization and habituation (28). The present study provides, however, the first indication for activity-dependent bidirectional plasticity in the neuronal excitability of central mammalian neurons.…”

Section: Discussionmentioning

confidence: 57%

Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons

Daoudal

Hanada

Debanne

2002

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

137

152

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Integration of synaptic excitation to generate an action potential (excitatory postsynaptic potential-spike coupling or E-S coupling) determines the neuronal output. Bidirectional synaptic plasticity is well established in the hippocampus, but whether active synaptic integration can display potentiation and depression remains unclear. We show here that synaptic depression is associated with an N-methyl-D-aspartate receptor-dependent and long-lasting depression of E-S coupling. E-S depression is input-specific and is expressed in the presence of ␥-aminobutyric acid type A and B receptor antagonists. In single neurons, E-S depression is observed without modification of postsynaptic passive properties. We conclude that a decrease in intrinsic excitability underlies E-S depression and is synergic with glutamatergic long-term depression.I ntegration of synaptic inputs to produce an action potential at the axon hillock is a complex operation that depends on two critical factors: the distribution of voltage-gated ion channels in the dendrites and the passive electrical properties upon which these active channels are superimposed (1). Synaptic potentials have been shown to be shaped by intrinsic voltage-gated conductances located in the dendrites and the soma (2), but the dynamics of active synaptic integration remains poorly understood. We addressed here the question as to whether synaptic integration is modified after induction of long-term synaptic potentiation and depotentiation.In the area CA1, homosynaptic long-term potentiation (LTP) of excitatory synaptic transmission is induced by high-frequency stimulation (HFS, 100 Hz) of the afferent fibers (3). In parallel, the probability of discharge of the postsynaptic neurons in response to a given excitatory postsynaptic potential (EPSP) is enhanced (4-7). This second component has been called EPSPto-Spike potentiation (E-S potentiation, E-S P) which is complementary to LTP and functionally important. The reversal of LTP preserves a potential for network plasticity and appears essential for any model of memory (8). Long-term synaptic depotentiation has been reported in the area CA1 (9), but the reversal of E-S P has never been clearly established (10, 11). We show here that E-S depression (E-S D) is expressed concomitantly with long-term depression (LTD). E-S D is largely independent of synaptic inhibition but requires N-methyl-D-aspartate (NMDA) receptor (NMDAR) activation for its induction. We provide evidence for an activity-dependent decrease of the intrinsic excitability of CA1 pyramidal neurons that acts in synergy with LTD. MethodsSlice Preparation. Hippocampal slices (400 m) were obtained from 3-to 6-week-old rats according to institutional guidelines. Slices were cut in a solution (280 mM sucrose͞26 mM NaHCO 3 ͞10 mM D-glucose͞1.3 mM KCl͞1 mM CaCl 2 ͞10 mM MgCl 2 ), and were maintained for 1 h at room temperature in oxygenated (95% O 2 ͞5% CO 2 ) artificial cerebrospinal fluid (ACSF; 125 mM NaCl͞2.5 mM KCl͞0.8 mM NaH 2 PO 4 ͞26 mM NaHCO 3 ͞3 mM CaCl 2 ͞2 mM Mg...

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“…Such changes are usually at the level of individual synapses, both pre-and postsynaptic (Nicoll and Malenka, 1995;Roberts and Glanzman, 2003), although the intrinsic excitability of neurons may also be altered (Farley et al, 1983;Cleary et al, 1998;Gainutdinov et al, 1998;Burrell et al, 2001;Antonov et al, 2001;Daoudal and Debanne, 2003;Zhang and Linden, 2003;Zhang et al, 2004). Remarkably, in the leech the ablation or axotomy of a single neuron, the S-cell, in just one ganglion eliminates a form of non-associative learning, sensitization of reflexive shortening (Sahley et al, 1994;Modney et al, 1997;Burrell et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…Although S-cell firing is not required for reflexive shortening, following a sensitizing stimulus S-cells are more active, and more reliably so, during shortening in response to the test stimulus (Modney et al, 1997;Burrell et al, 2003). Both the capacity for sensitization and the increase in S-cell activity involve 5-HT (Ehrlich et al, 1992), which increases S-cell excitability (Burrell et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Neuronal competition for action potential initiation sites in a circuit controlling simple learning

2007

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The spatial and temporal patterns of action potential initiations were studied in a behaving leech preparation to determine the basis of increased firing that accompanies sensitization, a form of nonassociative learning requiring the S-interneurons. Little is known at the network level about mechanisms of behavioral sensitization. The S-interneurons, one in each ganglion and linked by electrical synapses with both neighbors to form a chain, are interposed between sensory and motor neurons. In sensitized preparations the strength of shortening is related to S-cell firing, which itself is the result of impulses initiating in several S-cells. Because the S-cells, as independent initiation sites, all contribute to activity in the chain, it was hypothesized that during sensitization, increased multi-site activity increased the chain's firing rate. However, it was found that during sensitization, the single site with the largest initiation rate, the S-cell in the stimulated segment, suppressed initiations in adjacent ganglia. Experiments showed this was both because (1) it received the earliest, greatest input and (2) the delayed synaptic input to the adjacent S-cells coincided with the action potential refractory period. A compartmental model of the S-cell and its inputs showed that a simple, intrinsic mechanism of inexcitability after each action potential may account for suppression of impulse initiations. Thus, a non-synaptic competition between neurons alters synaptic integration in the chain. In one mode, inputs to different sites sum independently, whereas in another, synaptic input to a single site precisely specifies the overall pattern of activity.

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Non-Associative Learning and Serotonin Induce Similar Bi-Directional Changes in Excitability of a Neuron Critical for Learning in the Medicinal Leech

Cited by 84 publications

References 61 publications

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

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

Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons

Neuronal competition for action potential initiation sites in a circuit controlling simple learning

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