The Functional Influence of Burst and Tonic Firing Mode on Synaptic Interactions in the Thalamus

Kim, Uhnoh; McCormick, David A.

doi:10.1523/jneurosci.18-22-09500.1998

Cited by 140 publications

(112 citation statements)

References 84 publications

(87 reference statements)

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“…1F). There was no voltage envelope below the bursts as in thalamic relay neurons (19). At even higher frequencies these bursts fused, leading to continuous spiking and a drop in CV ISI below 0.5 in five of eight cells tested above a cell-specific frequency.…”

Section: Resultsmentioning

confidence: 86%

Origin of intrinsic irregular firing in cortical interneurons

Stiefel

Englitz

Sejnowski

2013

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

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Cortical spike trains are highly irregular both during ongoing, spontaneous activity and when driven at high firing rates. There is uncertainty about the source of this irregularity, ranging from intrinsic noise sources in neurons to collective effects in large-scale cortical networks. Cortical interneurons display highly irregular spike times (coefficient of variation of the interspike intervals >1) in response to dc-current injection in vitro. This is in marked contrast to cortical pyramidal cells, which spike highly irregularly in vivo, but regularly in vitro. We show with in vitro recordings and computational models that this is due to the fast activation kinetics of interneuronal K + currents. This explanation holds over a wide parameter range and with Gaussian white, power-law, and OrnsteinUhlenbeck noise. The intrinsically irregular spiking of interneurons could contribute to the irregularity of the cortical network.inhibitory interneuron | bistability | neural noise | fluctuations | cortex W hen spike trains of cortical pyramidal neurons are recorded in vivo from the cortices of awake or sleeping cats (1-3) or awake monkeys (4), the interspike intervals (ISIs) are highly variable, with coefficients of variation (CV ISI = ISI SD/ISI mean) >1. However, when the main cortical excitatory (pyramidal) neurons are depolarized in vitro by injection of constant current to above firing threshold, their spike trains are substantially more regular (CV ISI <0.5). The irregularity of pyramidal neuron firing in vivo arises from the intense, ongoing, temporally correlated synaptic activity that bombards cortical neurons (1, 2, 5-7). The lower in vitro irregularity can be raised to in vivo levels by using fluctuating current injection (8), hyperosmolar solution (9), and a neuromodulatory mixture (10, 11).Computational models of irregular neuronal firing typically include network synaptic activity represented by stochastic aggregate processes. Fluctuating inputs have been represented by Brownian motion (12) or an Ornstein-Uhlenbeck process (8) in both single-and multicompartmental neuronal models (5). These are externally induced fluctuations and do not mechanistically explain the variety of irregular discharge patterns observed in cortical interneurons. In this study we combined in vitro recordings and computational models of cortical interneurons to show how neuronal conductances interact with the stochastic input to produce the variety of observed neuronal phenotypes. ResultsRecordings from Cortical Inhibitory Interneurons. Cortical GABAergic interneurons have a range of functions including the gating (13) and entrainment (14) of neuronal firing, dendritic integration (15), synaptic plasticity (16), and the generation of network oscillations (10, 11). There are several morphologically and physiologically distinct classes of interneurons (17).In contrast to pyramidal neurons, a constant current injected into mouse visual cortex layer 2/3 interneurons in vitro frequently produced a spike train with a CV ISI that substant...

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Section: Resultsmentioning

confidence: 86%

Origin of intrinsic irregular firing in cortical interneurons

Stiefel

Englitz

Sejnowski

2013

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

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“…Studies on thalamic relay neurons have shown that relatively small changes in membrane potential can have dramatic consequences on neuronal firing (McCormick and Pape, 1990;Kim and McCormick, 1998). The apparent decrement in the effect of NT-3 on APmax from P10 to P14 was surprising given that P8 base neurons responded robustly.…”

Section: Resultsmentioning

confidence: 99%

Unmasking of Spiral Ganglion Neuron Firing Dynamics by Membrane Potential and Neurotrophin-3

Crozier

Davis

2014

J. Neurosci.

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Type I spiral ganglion neurons have a unique role relative to other sensory afferents because, as a single population, they must convey the richness, complexity, and precision of auditory information as they shape signals transmitted to the brain. To understand better the sophistication of spiral ganglion response properties, we compared somatic whole-cell current-clamp recordings from basal and apical neurons obtained during the first 2 postnatal weeks from CBA/CaJ mice. We found that during this developmental time period neuron response properties changed from uniformly excitable to differentially plastic. Low-frequency, apical and high-frequency basal neurons at postnatal day 1 (P1)-P3 were predominantly slowly accommodating (SA), firing at low thresholds with little alteration in accommodation response mode induced by changes in resting membrane potential (RMP) or added neurotrophin-3 (NT-3). In contrast, P10 -P14 apical and basal neurons were predominately rapidly accommodating (RA), had higher firing thresholds, and responded to elevation of RMP and added NT-3 by transitioning to the SA category without affecting the instantaneous firing rate. Therefore, older neurons appeared to be uniformly less excitable under baseline conditions yet displayed a previously unrecognized capacity to change response modes dynamically within a remarkably stable accommodation framework. Because the soma is interposed in the signal conduction pathway, these specializations can potentially lead to shaping and filtering of the transmitted signal. These results suggest that spiral ganglion neurons possess electrophysiological mechanisms that enable them to adapt their response properties to the characteristics of incoming stimuli and thus have the capacity to encode a wide spectrum of auditory information.

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“…5B). This happened because the slow EPSP decay time constant in RS and SOM cells (Table 2), relative to the short intraburst ISIs, enabled temporal summation (Kim and McCormick, 1998;Usrey et al, 2000) and also (in SOM cells) because of the absence, on average, of short-term depression (Figs. 1R, 3L;Beierlein et al, 2003;Minneci et al, 2007;Tan et al, 2008;Takesian et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…The combined result is that the first spike in the burst will activate a relatively undepressed synapse and elicit a considerably larger excitatory response compared with the average single spike (Swadlow and Gusev, 2001). Bursts could also enhance the postsynaptic response through temporal summation, when successively arriving EPSPs accumulate faster than they can dissipate (Kim and McCormick, 1998;Usrey et al, 2000). Conversely, high-frequency firing causes strong short-term depression of many thalamocortical synapses (Galarreta and Hestrin, 1998;González-Burgos et al, 2004;Gabernet et al, 2005;Kloc and Maffei, 2014), counteracting temporal summation.…”

Section: Introductionmentioning

confidence: 99%

Differential Excitation of Distally versus Proximally Targeting Cortical Interneurons by Unitary Thalamocortical Bursts

Agmon

2016

Journal of Neuroscience

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Thalamocortical neurons relay sensory and motor information to the neocortex using both single spikes and bursts; bursts prevail during low-vigilance states but also occur during awake behavior. Bursts are suggested to provide an alerting signal to the cortex and enhance stimulus detection, but the synaptic mechanisms underlying these effects are not clear, because the postsynaptic responses of different subtypes of cortical neurons to unitary thalamocortical bursts are mostly unknown. Using optogenetically guided recordings in mouse thalamocortical slices, we achieved the first reported paired intracellular recordings from nine monosynaptically connected thalamic and cortical neurons, including principal cells and two subtypes of inhibitory interneurons, and compared between cortical responses to single thalamocortical spikes and bursts. In 18 additional cortical neurons, we elicited unitary burst responses optogenetically. Shortterm dynamics and temporal summation of burst-evoked EPSPs were cell-type dependent: in principal cells and somatostatin-containing (SOM), but not fast-spiking (FS), interneurons, peak response during a burst was on average more than twofold larger than the response to the first spike. Thus, firing a burst instead of a single spike would more than double the probability of firing in postsynaptic excitatory neurons and in SOM, but not FS, interneurons. Consistent with this prediction, FS interneurons held near firing threshold fired most often on the first burst component, whereas SOM interneurons fired only on the second or later components. By increasing excitation of principal cells together with SOM-mediated, distally directed inhibition, thalamocortical bursts could momentarily enhance the saliency of the ascending sensory stimulus over less urgent, top-down inputs.

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The Functional Influence of Burst and Tonic Firing Mode on Synaptic Interactions in the Thalamus

Cited by 140 publications

References 84 publications

Origin of intrinsic irregular firing in cortical interneurons

Origin of intrinsic irregular firing in cortical interneurons

Unmasking of Spiral Ganglion Neuron Firing Dynamics by Membrane Potential and Neurotrophin-3

Differential Excitation of Distally versus Proximally Targeting Cortical Interneurons by Unitary Thalamocortical Bursts

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