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The BK-mediated fAHP is modulated by learning a hippocampus-dependent task.

ABSTRACT: Intrinsic excitability is a plastic property of cells that, along with synaptic changes, can be modulated by learning. Action potential (AP) height, width, and frequency are intrinsically controlled properties which rely on the activation of Na(+), Ca(2+), and K(+) channels in the dendritic, somatic, and axonal membranes. The fast after-hyperpolarization (fAHP) after an AP is partially responsible for determining the half-width and duration of the AP and thus Ca(2+) influx during the depolarization. In CA1 hippocampal pyramidal cells, the fAHP is carried by the voltage- and Ca(2+)-dependent BK channel. In addition to modulating the duration of the AP, the BK-mediated potassium current exerts control over the frequency of AP generation in response to a depolarizing input. These facts position BK-mediated effects to not only modulate immediate intraneuronal communication, but also to control longer-term Ca(2+)-dependent changes in the neuron, such as kinase activation, gene transcription, and synaptic plasticity. We examined how the BK-mediated fAHP was altered in hippocampal neurons after learning trace eyeblink conditioning. By using current clamp methods, it was found that the fAHP is reduced and the AP duration is increased in cells from conditioned animals. Additionally, in vitro and in vivo measures of firing frequency show that BK-channel blockade increases both evoked (in vitro) and spontaneous (in vivo) firing frequency of CA1 neurons, implicating the BK channel in the control of intrinsic excitability. These data indicate that the reduction of the BK-mediated fAHP is an essential part of the total increase of neuronal excitability known to accompany hippocampus-dependent learning.

SUBMITTER: Matthews EA

PROVIDER: S-EPMC2567507 | biostudies-other | 2008 Sep

REPOSITORIES: biostudies-other

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The BK-mediated fAHP is modulated by learning a hippocampus-dependent task.

Matthews Elizabeth A EA Weible Aldis P AP Shah Samit S Disterhoft John F JF

Proceedings of the National Academy of Sciences of the United States of America 20080917 39

Intrinsic excitability is a plastic property of cells that, along with synaptic changes, can be modulated by learning. Action potential (AP) height, width, and frequency are intrinsically controlled properties which rely on the activation of Na(+), Ca(2+), and K(+) channels in the dendritic, somatic, and axonal membranes. The fast after-hyperpolarization (fAHP) after an AP is partially responsible for determining the half-width and duration of the AP and thus Ca(2+) influx during the depolarizat ...[more]

PMID: 18799739

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Project description:Humans and non-human animals show great flexibility in spatial navigation, including the ability to return to specific locations based on as few as one single experience. To study spatial navigation in the laboratory, watermaze tasks, in which rats have to find a hidden platform in a pool of cloudy water surrounded by spatial cues, have long been used. Analogous tasks have been developed for human participants using virtual environments. Spatial learning in the watermaze is facilitated by the hippocampus. In particular, rapid, one-trial, allocentric place learning, as measured in the delayed-matching-to-place variant of the watermaze task, which requires rodents to learn repeatedly new locations in a familiar environment, is hippocampal dependent. In this article, we review some computational principles, embedded within a reinforcement learning framework, that utilise hippocampal spatial representations for navigation in watermaze tasks. We consider which key elements underlie their efficacy, and discuss their limitations in accounting for hippocampus-dependent navigation, both in terms of behavioural performance (i.e. how well do they reproduce behavioural measures of rapid place learning) and neurobiological realism (i.e. how well do they map to neurobiological substrates involved in rapid place learning). We discuss how an actor-critic architecture, enabling simultaneous assessment of the value of the current location and of the optimal direction to follow, can reproduce one-trial place learning performance as shown on watermaze and virtual delayed-matching-to-place tasks by rats and humans, respectively, if complemented with map-like place representations. The contribution of actor-critic mechanisms to delayed-matching-to-place performance is consistent with neurobiological findings implicating the striatum and hippocampo-striatal interaction in delayed-matching-to-place performance, given that the striatum has been associated with actor-critic mechanisms. Moreover, we illustrate that hierarchical computations embedded within an actor-critic architecture may help to account for aspects of flexible spatial navigation. The hierarchical reinforcement learning approach separates trajectory control via a temporal-difference error from goal selection via a goal prediction error and may account for flexible, trial-specific, navigation to familiar goal locations, as required in some arm-maze place memory tasks, although it does not capture one-trial learning of new goal locations, as observed in open field, including watermaze and virtual, delayed-matching-to-place tasks. Future models of one-shot learning of new goal locations, as observed on delayed-matching-to-place tasks, should incorporate hippocampal plasticity mechanisms that integrate new goal information with allocentric place representation, as such mechanisms are supported by substantial empirical evidence.

Dataset Information

The BK-mediated fAHP is modulated by learning a hippocampus-dependent task.

Publications

The BK-mediated fAHP is modulated by learning a hippocampus-dependent task.

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