Current-evoked transcellular K+ flux in frog retina

Karwoski, Chester J.; Coles, Jonathan A.; Lu, Hong-Kai; Huang, Bo

doi:10.1152/jn.1989.61.5.939

Cited by 13 publications

(5 citation statements)

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“…The main protagonists involved are K + channels (Orkand et al, 1966; Karwoski et al, 1989; Meeks and Mennerick, 2007), glutamate and GABA transporters (Bergles and Jahr, 1997; Diamond et al, 1998; Lüscher et al, 1998; Goubard et al, 2011), as well as AMPA receptor currents in Bergmann glial cells (Clark and Barbour, 1997; Bellamy and Ogden, 2006). As discussed above, K + currents are crucial to maintain the astrocyte at a markedly negative resting membrane potential, as well as for K + clearance during and after neuronal activity.…”

Section: Deciphering Neuroglial Interactions Using Astrocyte-neuron Dmentioning

confidence: 99%

How do astrocytes shape synaptic transmission? Insights from electrophysiology

Dallérac¹,

Chever²,

Rouach³

2013

Front. Cell. Neurosci.

145

117

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A major breakthrough in neuroscience has been the realization in the last decades that the dogmatic view of astroglial cells as being merely fostering and buffering elements of the nervous system is simplistic. A wealth of investigations now shows that astrocytes actually participate in the control of synaptic transmission in an active manner. This was first hinted by the intimate contacts glial processes make with neurons, particularly at the synaptic level, and evidenced using electrophysiological and calcium imaging techniques. Calcium imaging has provided critical evidence demonstrating that astrocytic regulation of synaptic efficacy is not a passive phenomenon. However, given that cellular activation is not only represented by calcium signaling, it is also crucial to assess concomitant mechanisms. We and others have used electrophysiological techniques to simultaneously record neuronal and astrocytic activity, thus enabling the study of multiple ionic currents and in depth investigation of neuro-glial dialogues. In the current review, we focus on the input such approach has provided in the understanding of astrocyte-neuron interactions underlying control of synaptic efficacy.

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Section: Deciphering Neuroglial Interactions Using Astrocyte-neuron Dmentioning

confidence: 99%

How do astrocytes shape synaptic transmission? Insights from electrophysiology

Dallérac¹,

Chever²,

Rouach³

2013

Front. Cell. Neurosci.

145

117

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“…Astrocytic processes enwrap more than half of CA1 hippocampal synapses to form tripartite synapses [ 1 , 2 ]. Perisynaptic astroglial processes are enriched in ionic channels, neurotransmitter receptors and transporters, enabling astrocytes to detect neuronal activity via calcium signaling [ 3 ] and ionic currents with various components, such as glutamate and GABA transporter [ 4 – 7 ] or potassium (K + ) [ 8 – 10 ]. Thus astrocytes regulate neuronal activity through multiple mechanisms, involving signaling or homeostasis of extracellular space volume, glutamate, GABA or K + levels [ 11 ].…”

Section: Introductionmentioning

confidence: 99%

The Neuroglial Potassium Cycle during Neurotransmission: Role of Kir4.1 Channels

et al. 2015

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Neuronal excitability relies on inward sodium and outward potassium fluxes during action potentials. To prevent neuronal hyperexcitability, potassium ions have to be taken up quickly. However, the dynamics of the activity-dependent potassium fluxes and the molecular pathways underlying extracellular potassium homeostasis remain elusive. To decipher the specific and acute contribution of astroglial Kir4.1 channels in controlling potassium homeostasis and the moment to moment neurotransmission, we built a tri-compartment model accounting for potassium dynamics between neurons, astrocytes and the extracellular space. We here demonstrate that astroglial Kir4.1 channels are sufficient to account for the slow membrane depolarization of hippocampal astrocytes and crucially contribute to extracellular potassium clearance during basal and high activity. By quantifying the dynamics of potassium levels in neuron-glia-extracellular space compartments, we show that astrocytes buffer within 6 to 9 seconds more than 80% of the potassium released by neurons in response to basal, repetitive and tetanic stimulations. Astroglial Kir4.1 channels directly lead to recovery of basal extracellular potassium levels and neuronal excitability, especially during repetitive stimulation, thereby preventing the generation of epileptiform activity. Remarkably, we also show that Kir4.1 channels strongly regulate neuronal excitability for slow 3 to 10 Hz rhythmic activity resulting from probabilistic firing activity induced by sub-firing stimulation coupled to Brownian noise. Altogether, these data suggest that astroglial Kir4.1 channels are crucially involved in extracellular potassium homeostasis regulating theta rhythmic activity.

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“…In contrast, although glial membrane depolarization was the first activity-dependent signal identified (Orkand et al 1966), the ionic responses of astrocytes received less attention, because of their slower time scale, the passive glial membrane properties and the lack of selective pharmacological tools to investigate their functional consequences. Nevertheless, neuronal activity induces in glial cells ionic currents with various components in different brain regions, such as potassium currents (Orkand et al 1966;Karwoski et al 1989;Meeks & Mennerick, 2007), glutamate and GABA transporter (GLT, GAT) currents (Bergles & Jahr, 1997;Diamond et al 1998;Luscher et al 1998;Goubard et al 2011), or AMPA receptor (AMPAR) currents in cerebellar Bergmann glia (Clark & Barbour, 1997;Bellamy & Ogden, 2005).…”

Section: Introductionmentioning

confidence: 99%

Astroglial potassium clearance contributes to short‐term plasticity of synaptically evoked currents at the tripartite synapse

Sibille

Pannasch

Rouach

2013

The Journal of Physiology

132

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Key points• Astrocytes, active players in neurotransmission, display complex membrane ionic responses upon neuronal activity.• However, the nature, plasticity and role of the activity-dependent astroglial currents on synaptic plasticity remain unclear in the hippocampus.• We here demonstrate, using simultaneous electrophysiological recordings of hippocampal neurons and astrocytes, that the complex astroglial current induced synaptically is dominated (80%) by potassium entry through K ir 4.1 channels and also includes, in addition to the glutamate transporter current, a small residual current, partially mediated by GABA transporters and K ir 4.1-independent potassium channels.• These synaptically evoked astroglial currents exhibit differential short-term plasticity patterns, and astroglial potassium uptake mediated by K ir 4.1 channels down-regulates hippocampal short-term plasticity.• This study establishes astrocytes as integrators of excitatory and inhibitory synaptic activity, which may, through dynamic potassium handling, define the signal-to-noise ratio essential for specific strengthening of synaptic contacts and synchronization of neuronal ensembles, a prerequisite for learning and memory.Abstract Astroglial processes enclose ∼60% of CA1 hippocampal synapses to form the tripartite synapse. Although astrocytes express ionic channels, neurotransmitter receptors and transporters to detect neuronal activity, the nature, plasticity and impact of the currents induced by neuronal activity on short-term synaptic plasticity remain elusive in hippocampal astrocytes. Using simultaneous electrophysiological recordings of astrocytes and neurons, we found that single stimulation of Schaffer collaterals in hippocampal slices evokes in stratum radiatum astrocytes a complex prolonged inward current synchronized to synaptic and spiking activity in CA1 pyramidal cells. The astroglial current is composed of three components sensitive to neuronal activity, i.e. a long-lasting potassium current mediated by K ir 4.1 channels, a transient glutamate transporter current and a slow residual current, partially mediated by GABA transporters and K ir 4.1-independent potassium channels. We show that all astroglial membrane currents exhibit activity-dependent short-term plasticity. However, only the astroglial glutamate transporter current displays neuronal-like dynamics and plasticity. As K ir 4.1 channel-mediated potassium uptake contributes to 80% of the synaptically evoked astroglial current, we investigated in turn its impact on short-term synaptic plasticity. Using glial conditional K ir 4.1 knockout mice, we found that astroglial potassium uptake reduces synaptic responses to repetitive stimulation and post-tetanic potentiation. These results show that astrocytes integrate synaptic activity via multiple ionic channels and transporters and contribute to short-term plasticity in part via potassium clearance mediated by K ir 4.1 channels.

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Current-evoked transcellular K+ flux in frog retina

Cited by 13 publications

References 0 publications

How do astrocytes shape synaptic transmission? Insights from electrophysiology

How do astrocytes shape synaptic transmission? Insights from electrophysiology

The Neuroglial Potassium Cycle during Neurotransmission: Role of Kir4.1 Channels

Astroglial potassium clearance contributes to short‐term plasticity of synaptically evoked currents at the tripartite synapse

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