NMDA Spike/Plateau Potentials in Dendrites of Thalamocortical Neurons

Augustinaite, Sigita; Kühn, Bernd; Helm, P. Johannes; Heggelund, Paul

doi:10.1523/jneurosci.1205-13.2014

Cited by 28 publications

(46 citation statements)

References 54 publications

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“…The apparent nonlinearity, manifested by the strong inward currents recorded near spike threshold, could be caused by the activation of N -methyl-D-aspartate receptors (NMDARs). In fact, NMDARs are present at the CT-VPm synapse (Deschenes and Hu, 1990; Kao and Coulter, 1997; Miyata, 2007; Pedroarena and Llinás, 2001; Scharfman et al, 1990), and there is evidence that NMDA spikes can be elicited in distal dendrites of thalamic relay cells, where the majority of CT terminals are located (Augustinaite et al, 2014; Liu et al, 1995). …”

Section: Resultsmentioning

confidence: 99%

A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

Crandall

Cruikshank

Connors

2015

Neuron

278

314

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SUMMARY Corticothalamic neurons provide massive input to the thalamus. This top-down projection may allow cortex to regulate sensory processing by modulating the excitability of thalamic cells. Layer 6 corticothalamic neurons monosynaptically excite thalamocortical cells, but also indirectly inhibit them by driving inhibitory cells of the thalamic reticular nucleus. Whether corticothalamic activity generally suppresses or excites the thalamus remains unclear. Here we show that the corticothalamic influence is dynamic, with the excitatory-inhibitory balance shifting in an activity-dependent fashion. During low-frequency activity corticothalamic effects are mainly suppressive, whereas higher frequency activity (even a short bout of gamma frequency oscillations) converts the corticothalamic influence to enhancement. The mechanism of this switching depends upon distinct forms of short-term synaptic plasticity across multiple corticothalamic circuit components. Our results reveal an activity-dependent mechanism by which corticothalamic neurons can bidirectionally switch the excitability and sensory throughput of the thalamus, possibly to meet changing behavioral demands.

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Section: Resultsmentioning

confidence: 99%

A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

Crandall

Cruikshank

Connors

2015

Neuron

278

314

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“…by lifting the cell body membrane potential toward the threshold for action potential generation, and thereby increasing the probability for spike generation by the synaptic input from the retinal afferents (Augustinaite et al, 2014 Interestingly, dependence of dT on the Vm-t was very similar between "induced voltage change" and "plateau" (Fig. 9H) despite the fact that TAU differed across these 2 conditions.…”

Section: Distortion Of the Neuronal R In And Tau By Simple Depolarizamentioning

confidence: 90%

“…As glutamate input location is moved away from the soma, somatic plateau depolarization amplitude decreases rapidly (Milojkovic et al, 2004;Major et al, 2008;Augustinaite et al, 2014). This "distance-dependence" segregates roughly the basal dendrite into proximal and distal region --only proximal dendritic segments will generate APs on the somatic plateau (Fig.…”

Section: Spikeless Plateaus Begin In the Middle Of The Basal Dendritementioning

confidence: 92%

Local Glutamate-Mediated Dendritic Plateau Potentials Change the State of the Cortical Pyramidal Neuron

Gao

Graham

Zhou

et al. 2019

Preprint

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37Dendritic spikes in thin dendritic branches (basal and oblique dendrites) of pyramidal neurons 38 are traditionally inferred from spikelets measured in the cell body. Here, we used laser-spot 39 voltage-sensitive dye imaging in cortical pyramidal neurons (rat brain slices) to investigate the 40 voltage waveforms of dendritic potentials occurring in response to spatially-restricted 41 glutamatergic inputs. Local dendritic potentials lasted 200-500 ms and propagated to the cell 42 body where they caused sustained 10-20 mV depolarizations. Plateau potentials propagating 43 from dendrite to soma, and action potentials propagating from soma to dendrite, created 44 complex voltage waveforms in the middle of the thin basal dendrite, comprised of local sodium 45 spikelets, local plateau potentials, and back-propagating action potentials, superimposed on 46 each other. Our model replicated these experimental observations and made the following 47 predictions: (i) membrane time constant is shortened during the plateau; and (ii) synaptic 48 responses are more effective drivers of neuronal action potentials during the plateau potential.49 Dendritic plateau potentials occurring in basal and oblique branches put pyramidal neurons into 50 an activated neuronal state ("prepared state"), characterized by depolarized membrane potential 51 and notably faster membrane responses. The prepared state provides a time window of 200-52 500 ms during which cortical neurons are particularly excitable and capable of following afferent 53 inputs. At the network level, this predicts that sets of cells with simultaneous plateaus would 54 provide cellular substrate for the formation of functional neuronal ensembles. 55 56 57 58 59Significance statement: Strong and clustered glutamatergic inputs will have a major 60 influence on activity at both neuronal and network scales. We recorded glutamate-mediated 61 dendritic voltage plateaus using voltage imaging, and created a computer model that recreated 62 experimental measures. Our model predicts the manner in which plateaus are triggered and the 63 impact of inputs to an individual thin dendrite on the membrane response in the cell body. 64 Plateau potentials profoundly change neuronal state --a plateau potential triggered in one basal 65 dendrite depolarizes the soma and shortens membrane time constant, making the cell more 66 susceptible to firing triggered by other afferent inputs. We tested model predictions 67 experimentally. 68 69 70 The individual spiny neuron is subjected to a variety of excitatory input patterns, often resulting 71 from concurrent release across multiple synapses on a single dendrite. Due to combinations of 72 temporal and spatial clustering 1-3 , the amount of glutamate released on a single basilar dendrite 73 can be quite large, potentially spilling over to extrasynaptic NMDA receptors, and temporarily 74 overwhelming the ability of astrocytes to fully compensate. In vitro focal applications of 75 comparable amounts of glutamate, or repetitive synaptic stimulations, wi...

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“…Moreover, the cortical feedback can elicit long‐lasting dendritic plateau potentials in TC neurons that may further boost the transmission of retinal signals through dLGN (Augustinaite et al . ). The results from the present study clearly demonstrate that SynI can play important roles in the effects of the cortical feedback in thalamus.…”

Section: Discussionmentioning

confidence: 97%

Functions of synapsins in corticothalamic facilitation: important roles of synapsin I

Nikolaev

Heggelund

2015

The Journal of Physiology

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Key pointsr The synaptic vesicle associated proteins synapsin I and synapsin II have important functions in synaptic short-term plasticity.r We investigated their functions in cortical facilitatory feedback to neurons in dorsal lateral geniculate nucleus (dLGN), feedback that has important functions in state-dependent regulation of thalamic transmission of visual input to cortex.r We compared results from normal wild-type (WT) mice and synapsin knockout (KO) mice in several types of synaptic plasticity, and found clear differences between the responses of neurons in the synapsin I KO and the WT, but no significant differences between the synapsin II KO and the WT. AbstractThe synaptic vesicle associated proteins synapsin I (SynI) and synapsin II (SynII) have important functions in several types of synaptic short-term plasticity in the brain, but their separate functions in different types of synapses are not well known. We investigated possible distinct functions of the two synapsins in synaptic short-term plasticity at corticothalamic synapses on relay neurons in the dorsal lateral geniculate nucleus. These synapses provide excitatory feedback from visual cortex to the relay cells, feedback that can facilitate transmission of signals from retina to cortex. We compared results from normal wild-type (WT), SynI knockout (KO) and SynII KO mice, in three types of synaptic plasticity mainly linked to presynaptic mechanism. In SynI KO mice, paired-pulse stimulation elicited increased facilitation at short interpulse intervals compared to the WT. Pulse-train stimulation elicited weaker facilitation than in the WT, and also post-tetanic potentiation was weaker in SynI KO than in the WT. Between SynII KO and the WT we found no significant differences. Thus, SynI has important functions in these types of synaptic plasticity at corticothalamic synapses. Interestingly, our data are in contrast to the important role of SynII previously shown for sustained synaptic transmission during intense stimulation in excitatory synapses in other parts of the brain, and our results suggest that SynI and SynII may have different roles in similar types of STP in different parts of the brain.

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NMDA Spike/Plateau Potentials in Dendrites of Thalamocortical Neurons

Cited by 28 publications

References 54 publications

A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

A Corticothalamic Switch: Controlling the Thalamus with Dynamic Synapses

Local Glutamate-Mediated Dendritic Plateau Potentials Change the State of the Cortical Pyramidal Neuron

Functions of synapsins in corticothalamic facilitation: important roles of synapsin I

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