In Vivo Dynamic-Clamp Manipulation of Extrinsic and Intrinsic Conductances: Functional Roles of Shunting Inhibition and I BK in Rat and Cat Cortex

Graham, Lyle J.; Schramm, Adrien E.

doi:10.1007/978-0-387-89279-5_7

Cited by 9 publications

(6 citation statements)

References 44 publications

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“…In contrast, results from in vivo recordings from rat cortex indicate that an inhibitory conductance implemented with dynamic clamp without noise can divisively scale the output of principle neurons showing spike frequency adaptation (Graham and Schramm, 2009). This is further supported by in vivo recordings of cat cortical neurons showing that under noisy conditions the gain of the neuron changes only when the membrane resistance decreases (Cardin et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

Gain Control in CA1 Pyramidal Cells Using Changes in Somatic Conductance

Fernandez¹,

White²

2010

J. Neurosci.

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Gain modulation is an important feature of neural activity. Previous work has focused on the ability of background synaptic noise to modulate the slope (i.e., gain) of the frequency-current ( f-I) relationship in neurons. To date, demonstrations of gain control that are independent of synaptic noise have been limited. We investigated the effects of increasing somatic conductance in the form of tonic inhibition on the initial and steady-state f-I relationship of CA1 pyramidal cells. We find that increasing membrane conductance reduces the gain of the steady-state f-I relationship through a graded increase in the magnitude of spike frequency adaptation. Increased adaptation arises through a conductance-induced depolarization of spike voltage threshold. Thus, by increasing the magnitude of spike frequency adaptation, added conductance can reduce the gain of the steady-state f-I relationship in the absence of random background membrane fluctuations.

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Section: Discussionmentioning

confidence: 99%

Gain Control in CA1 Pyramidal Cells Using Changes in Somatic Conductance

Fernandez¹,

White²

2010

J. Neurosci.

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“…Some have reported a divisive effect from background synaptic noise (Chance et al 2002;Mitchell and Silver 2003;Prescott and De Koninck 2003), whereas others have shown either a multiplicative effect or a mixture of effects across cell types (Higgs et al 2006;Murphy and Miller 2003). Barrages of synaptic activity as seen in vivo would induce conductance changes without additional DC current steps (Graham and Schramm 2009). Therefore we measured the response gain resulting from noisy conductance steps without an additional DC step to simulate biologically realistic synaptic stimulation.…”

Section: Discussionmentioning

confidence: 99%

Modulation of Firing Rate by Background Synaptic Noise Statistics in Rat Visual Cortical Neurons

Sceniak

Sabo

2010

Journal of Neurophysiology

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It has been shown previously that background synaptic noise modulates the response gain of neocortical neurons. However, the role of the statistical properties of the noise in modulating firing rate is not known. Here, the dependence of firing rate on the statistical properties of the excitatory to inhibitory balance (EI) in cortical pyramidal neurons was studied. Excitatory glutamatergic and inhibitory GABAergic synaptic conductances were simulated as two stochastic processes and injected into individual neurons in vitro through use of the dynamic-clamp system. Response gain was significantly modulated as a function of the statistical interactions between excitatory and inhibitory synaptic conductances. Firing rates were compared for noisy synaptic conductance steps by varying either the EI correlation or the relative delay between correlated E and I. When inhibitory synaptic conductances exhibited a short temporal delay (5 ms) relative to correlated excitatory synaptic conductances, the response gain was increased compared with noise with no temporal delay but with an equivalent degree of correlation. The dependence of neuronal firing rate on the EI delay of the noisy background synaptic conductance suggests that individual excitatory pyramidal neurons are sensitive to the EI balance of the synaptic conductance. Therefore the statistical EI interactions encoded within the synaptic subthreshold membrane fluctuations are able to modulate neuronal firing properties.

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“…Using a voltage window (Graham and Schramm 2009), we limited the activation of the modeled K ϩ current to the fAHP component of the AP waveform. The calculated current was added to or subtracted from the injected current, and the sum is then passed to the currentclamp amplifier where the total current injected in the cell is adjusted in real time.…”

Section: Methodsmentioning

confidence: 99%

Knockout of the BK β₄-subunit promotes a functional coupling of BK channels and ryanodine receptors that mediate a fAHP-induced increase in excitability

Wang

Bugay

Ling

et al. 2016

Journal of Neurophysiology

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Knockout of the BK ␤ 4 -subunit promotes a functional coupling of BK channels and ryanodine receptors that mediate a fAHP-induced increase in excitability. J Neurophysiol 116: 456 -465, 2016. First published May 4, 2016 doi:10.1152/jn.00857.2015.-BK channels are large-conductance calcium-and voltage-activated potassium channels with diverse properties. Knockout of the accessory BK ␤ 4 -subunit in hippocampus dentate gyrus granule neurons causes BK channels to change properties from slow-gated type II channels to fast-gated type I channels that sharpen the action potential, increase the fast afterhyperpolarization (fAHP) amplitude, and increase spike frequency. Here we studied the calcium channels that contribute to fast-gated BK channel activation and increased excitability of ␤ 4 knockout neurons. By using pharmacological blockers during currentclamp recording, we find that BK channel activation during the fAHP is dependent on ryanodine receptor activation. In contrast, L-type calcium channel blocker (nifedipine) affects the BK channel-dependent repolarization phase of the action potential but has no effect on the fAHP. Reducing BK channel activation during the repolarization phase with nifedipine, or during the fAHP with ryanodine, indicated that it is the BK-mediated increase of the fAHP that confers proexcitatory effects. The proexcitatory role of the fAHP was corroborated using dynamic current clamp. Increase or decrease of the fAHP amplitude during spiking revealed an inverse relationship between fAHP amplitude and interspike interval. Finally, we show that the seizure-prone ryanodine receptor gain-of-function (R2474S) knockin mice have an unaltered repolarization phase but larger fAHP and increased AP frequency compared with their control littermates. In summary, these results indicate that an important role of the ␤ 4 -subunit is to reduce ryanodine receptor-BK channel functional coupling during the fAHP component of the action potential, thereby decreasing excitability of dentate gyrus neurons.large-conductance calcium-and voltage-activated potassium channels; action potentials; dentate gyrus; fast afterhyperpolarization

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In Vivo Dynamic-Clamp Manipulation of Extrinsic and Intrinsic Conductances: Functional Roles of Shunting Inhibition and I BK in Rat and Cat Cortex

Cited by 9 publications

References 44 publications

Gain Control in CA1 Pyramidal Cells Using Changes in Somatic Conductance

Gain Control in CA1 Pyramidal Cells Using Changes in Somatic Conductance

Modulation of Firing Rate by Background Synaptic Noise Statistics in Rat Visual Cortical Neurons

Knockout of the BK β₄-subunit promotes a functional coupling of BK channels and ryanodine receptors that mediate a fAHP-induced increase in excitability

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In Vivo Dynamic-Clamp Manipulation of Extrinsic and Intrinsic Conductances: Functional Roles of Shunting Inhibition and I BK in Rat and Cat Cortex

Cited by 9 publications

References 44 publications

Gain Control in CA1 Pyramidal Cells Using Changes in Somatic Conductance

Gain Control in CA1 Pyramidal Cells Using Changes in Somatic Conductance

Modulation of Firing Rate by Background Synaptic Noise Statistics in Rat Visual Cortical Neurons

Knockout of the BK β4-subunit promotes a functional coupling of BK channels and ryanodine receptors that mediate a fAHP-induced increase in excitability

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Knockout of the BK β₄-subunit promotes a functional coupling of BK channels and ryanodine receptors that mediate a fAHP-induced increase in excitability