Cell type‐specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones

Lawrence, J. Josh; Statland, Jeffrey; Grinspan, Zachary M.; McBain, Chris J.

doi:10.1113/jphysiol.2005.100875

Cited by 106 publications

(140 citation statements)

References 60 publications

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“…10 D i ). Finally, the model is also consistent with published work (Lawrence et al, 2006a), indicating that linopirdine does not change the first spike latency when the cell is depolarized from Ϫ60 mV. At this voltage, I M is active by only 0.12%, contributing very little to R m or m .…”

Section: The Role Of G M In Shaping Interneuronal Ahp and Interspike supporting

confidence: 79%

“…The model also accounts, in part, for how g M can influence the ISI yet, paradoxically, have little effect on the amplitude of the AHP after a 1 s train of APs (Fig. 10C,D) (Lawrence et al, 2006a). When g M is inhibited, the accompanying increase in AP frequency (Fig.…”

Section: The Role Of G M In Shaping Interneuronal Ahp and Interspike mentioning

confidence: 99%

“…7), tetrodotoxin (1 M) was added and CsCl (5 mM) was replaced with equimolar NaCl in VC experiments to block Na ϩ channels and the hyperpolarization-activated current I h , respectively. For VC recordings in which strong depolarizing voltage steps were introduced, CaCl 2 was lowered to 0 -0.5 mM and MgCl 2 elevated to 2-4 mM to reduce the activation of a slow Ca 2ϩ -activated K ϩ conductance (Lawrence et al, 2006a). In some experiments, 50 M CdCl 2 or 2 mM EGTA was added to further reduce the influence of I AHP .…”

Section: Methodsmentioning

confidence: 99%

“…Although early immunocytochemical evidence indicated that Kv7 subunits were localized somatodendritically on hippocampal pyramidal cells (Cooper et al, 2000;Shah et al, 2002) and interneurons (Cooper et al, 2001), an additional population of Kv7 channels has been more recognized recently on the axon initial segment and nodes of Ranvier of CNS neurons (Devaux et al, 2004;Chung et al, 2006;Pan et al, 2006). Kv7 channel antagonists modulate axonal excitability (Devaux et al, 2004), raising uncertainty about whether axonal or dendritic Kv7 channels mediate I M -dependent changes in cellular excitability originally described in hippocampal pyramidal neurons (Yue and Yaari, 2004;Gu et al, 2005) and interneurons (Lawrence et al, 2006a).…”

Section: Introductionmentioning

confidence: 99%

“…Although interneurons are strongly activated by acetylcholine (McQuiston and Madison, 1999;Lawrence et al, 2006a) and possess numerous K ϩ conductances (Zhang and McBain, 1995a,b;Martina et al, 1998Martina et al, , 2000Lien et al, 2002;Lien and Jonas, 2003), the question of whether interneurons possess I M has received little attention. Recently, we demonstrated that oriens-lacunosum moleculare (O-LM) cells generate a large mAChR-dependent afterdepolarization that is partially dependent on I M inhibition (Lawrence et al, 2006a), but the nature of how I M itself impacts excitability in stratum oriens (SO) interneurons has not yet been explored in detail. Moreover, the cellular localization of Kv7 channels in neurons has recently become a point of interest.…”

Section: Introductionmentioning

confidence: 99%

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Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons

Lawrence

Saraga²,

Churchill³

et al. 2006

J. Neurosci.

178

163

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The M-current (I M ), comprised of Kv7 channels, is a voltage-activated K ϩ conductance that plays a key role in the control of cell excitability. In hippocampal principal cells, I M controls action potential (AP) accommodation and contributes to the medium-duration afterhyperpolarization, but the role of I M in control of interneuron excitability remains unclear. Here, we investigated I M in hippocampal stratum oriens (SO) interneurons, both from wild-type and transgenic mice in which green fluorescent protein (GFP) was expressed in somatostatin-containing interneurons. Somatodendritic expression of Kv7.2 or Kv7.3 subunits was colocalized in a subset of GFPϩ SO interneurons, corresponding to oriens-lacunosum moleculare (O-LM) cells. Under voltage clamp (VC) conditions at Ϫ30 mV, the Kv7 channel antagonists linopirdine/XE-991 abolished the I M amplitude present during relaxation from Ϫ30 to Ϫ50 mV and reduced the holding current (I hold ). In addition, 0.5 mM tetraethylammonium reduced I M , suggesting that I M was composed of Kv7.2-containing channels. In contrast, the Kv7 channel opener retigabine increased I M amplitude and I hold . When strongly depolarized in VC, the linopirdine-sensitive outward current activated rapidly and comprised up to 20% of the total current. In current-clamp recordings from GFPϩ SO cells, linopirdine induced depolarization and increased AP frequency, whereas retigabine induced hyperpolarization and arrested firing. In multicompartment O-LM interneuron models that incorporated I M , somatodendritic placement of Kv7 channels best reproduced experimentally measured I M . The models suggest that Kv3-and Kv7-mediated channels both rapidly activate during single APs; however, Kv3 channels control rapid repolarization of the AP, whereas Kv7 channels primarily control the interspike interval.

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Section: The Role Of G M In Shaping Interneuronal Ahp and Interspike supporting

confidence: 79%

Section: The Role Of G M In Shaping Interneuronal Ahp and Interspike mentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons

Lawrence

Saraga²,

Churchill³

et al. 2006

J. Neurosci.

178

163

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Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons

et al. 2006

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The hippocampus receives an extensive cholinergic input from the medial septal nucleus that ramifies throughout all layers and plays a pivotal modulatory role in cognitive function. Although the pharmacological effects of exogenous application of cholinergic agonists have been extensively studied in hippocampal neurons, much less is known about the effects of synaptically released acetylcholine (ACh). In this respect, most studies have focused on the cholinergic afferent input to pyramidal neurons that produces a characteristically slow depolarizing synaptic response mediated by activation of muscarinic ACh receptors (mAChRs). Here we report that cholinergic afferent stimulation also elicits atropine-sensitive synaptic potentials in hippocampal CA1 interneurons but, in contrast to synaptic responses in pyramidal neurons, these are highly diverse in waveform, although can still be classified into five distinct subtypes. The most common response type (i) 64% of cells) consisted of a slow sustained membrane potential depolarization. The other 36% of responses could be subdivided into responses comprising of (ii) a biphasic membrane potential change in which an initial slow hyperpolarization subsequently transforms into a slow depolarization (20%), (iii) a pure, slow hyperpolarization (13%), and (iv) an oscillatory response persisting for several seconds (2%). Interestingly, there were also interneurons totally insensitive to both synaptic and pharmacological cholinergic challenge. Morphological investigation of recorded cells revealed no obvious correlation between responsiveness to cholinergic afferent stimulation and dendritic and axonal arborization. The current study suggests that synaptic release of ACh results in a complex and differential mAChR-mediated modulation of cellular excitability within the hippocampal interneuron population.

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The race to learn: Spike timing and STDP can coordinate learning and recall in CA3

et al. 2011

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The CA3 region of the hippocampus has long been proposed as an autoassociative network performing pattern completion on known inputs. The dentate gyrus (DG) region is often proposed as a network performing the complementary function of pattern separation. Neural models of pattern completion and separation generally designate explicit learning phases to encode new information and assume an ideal fixed threshold at which to stop learning new patterns and begin recalling known patterns. Memory systems are significantly more complex in practice, with the degree of memory recall depending on context-specific goals. Here, we present our spike-timing separation and completion (STSC) model of the entorhinal cortex (EC), DG, and CA3 network, ascribing to each region a role similar to that in existing models but adding a temporal dimension by using a spiking neural network. Simulation results demonstrate that (a) spike-timing dependent plasticity in the EC-CA3 synapses provides a pattern completion ability without recurrent CA3 connections, (b) the race between activation of CA3 cells via EC-CA3 synapses and activation of the same cells via DG-CA3 synapses distinguishes novel from known inputs, and (c) modulation of the EC-CA3 synapses adjusts the learned versus test input similarity required to evoke a direct CA3 response prior to any DG activity, thereby adjusting the pattern completion threshold. These mechanisms suggest that spike timing can arbitrate between learning and recall based on the novelty of each individual input, ensuring control of the learn-recall decision resides in the same subsystem as the learned memories themselves. The proposed modulatory signal does not override this decision but biases the system toward either learning or recall. The model provides an explanation for empirical observations that a reduction in novelty produces a corresponding reduction in the latency of responses in CA3 and CA1.

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Cell type‐specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones

Cited by 106 publications

References 60 publications

Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons

Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons

Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons

The race to learn: Spike timing and STDP can coordinate learning and recall in CA3

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