State-Dependent Firing Determines Intrinsic Dendritic Ca<sup>2+</sup>Signaling in Thalamocortical Neurons

Errington, Adam C.; Renger, John J.; Uebele, Victor N.; Crunelli, Vincenzo

doi:10.1523/jneurosci.2968-10.2010

Cited by 38 publications

(73 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…When considered alongside our own previous studies (Errington et al, 2010, 2012; Connelly et al, 2015, 2016) and those of others (Crandall et al, 2010, Cueni et al, 2008, Chausson et al, 2013), these new findings allow us to build a more complete picture of the role that dendrites play in thalamic neuron electrogenesis and signaling.…”

Section: Discussionmentioning

confidence: 60%

Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons

2017

View full text Add to dashboard Cite

Backpropagating action potentials (bAPs) are indispensable in dendritic signaling. Conflicting Ca2+-imaging data and an absence of dendritic recording data means that the extent of backpropagation in thalamocortical (TC) and thalamic reticular nucleus (TRN) neurons remains unknown. Because TRN neurons signal electrically through dendrodendritic gap junctions and possibly via chemical dendritic GABAergic synapses, as well as classical axonal GABA release, this lack of knowledge is problematic. To address this issue, we made two-photon targeted patch-clamp recordings from rat TC and TRN neuron dendrites to measure bAPs directly. These recordings reveal that “tonic”' and low-threshold-spike (LTS) “burst” APs in both cell types are always recorded first at the soma before backpropagating into the dendrites while undergoing substantial distance-dependent dendritic amplitude attenuation. In TC neurons, bAP attenuation strength varies according to firing mode. During LTS bursts, somatic AP half-width increases progressively with increasing spike number, allowing late-burst spikes to propagate more efficiently into the dendritic tree compared with spikes occurring at burst onset. Tonic spikes have similar somatic half-widths to late burst spikes and undergo similar dendritic attenuation. In contrast, in TRN neurons, AP properties are unchanged between LTS bursts and tonic firing and, as a result, distance-dependent dendritic attenuation remains consistent across different firing modes. Therefore, unlike LTS-associated global electrical and calcium signals, the spatial influence of bAP signaling in TC and TRN neurons is more restricted, with potentially important behavioral-state-dependent consequences for synaptic integration and plasticity in thalamic neurons.SIGNIFICANCE STATEMENT In most neurons, action potentials (APs) initiate in the axosomatic region and propagate into the dendritic tree to provide a retrograde signal that conveys information about the level of cellular output to the locations that receive most input: the dendrites. In thalamocortical and thalamic reticular nucleus neurons, the site of AP generation and the true extent of backpropagation remain unknown. Using patch-clamp recordings, this study measures dendritic propagation of APs directly in these neurons. In either cell type, high-frequency low-threshold spike burst or lower-frequency tonic APs undergo substantial voltage attenuation as they spread into the dendritic tree. Therefore, backpropagating spikes in these cells can only influence signaling in the proximal part of the dendritic tree.

show abstract

Section: Discussionmentioning

confidence: 60%

Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons

2017

View full text Add to dashboard Cite

show abstract

“…The robustness of RD could partly be attributed to the high density of expression of T-type Ca 2? channels in the soma and dendrites of thalamic relay neurons [37][38][39]. Third, RD can be recorded in most MGB neurons in young animals (P15-22).…”

Section: Rd In Mgb Neurons Is Carried By T-type Ca 21 Channelsmentioning

confidence: 95%

Characterization of Rebound Depolarization in Neurons of the Rat Medial Geniculate Body In Vitro

et al. 2016

View full text Add to dashboard Cite

Rebound depolarization (RD) is a response to the offset from hyperpolarization of the neuronal membrane potential and is an important mechanism for the synaptic processing of inhibitory signals. In the present study, we characterized RD in neurons of the rat medial geniculate body (MGB), a nucleus of the auditory thalamus, using whole-cell patch-clamp and brain slices. RD was proportional in strength to the duration and magnitude of the hyperpolarization; was effectively blocked by Ni 2? or Mibefradil; and was depressed when the resting membrane potential was hyperpolarized by blocking hyperpolarization-activated cyclic nucleotide-gated (HCN) channels with ZD7288 or by activating G-protein-gated inwardly-rectifying K ? (GIRK) channels with baclofen. Our results demonstrated that RD in MGB neurons, which is carried by T-type Ca 2? channels, is critically regulated by HCN channels and likely by GIRK channels.

show abstract

“…Baseline levels of [Ca 2+ ] ranged from 50–80 nM in parafascicular thalamic neurons using bis-fura 2 [14]. Dendrites can actively sustain low frequency activity in thalamocortical neurons [9–11]. These authors showed dendritic [Ca 2+ ] dynamics (using fluorescence recordings of fluo-filled thalamocortical neurons) during repetitive low frequency spikes [10,11].…”

Section: Discussionmentioning

confidence: 99%

“…Dendrites can actively sustain low frequency activity in thalamocortical neurons [9–11]. These authors showed dendritic [Ca 2+ ] dynamics (using fluorescence recordings of fluo-filled thalamocortical neurons) during repetitive low frequency spikes [10,11]. Morever, ryanodine receptor-dependent Ca 2+ -induced Ca 2+ release [11,34], and Ca 2+ -dependent K + channel activation [42], might blunt the amplitude of [Ca 2+ ] mediated fluorescence signals.…”

Section: Discussionmentioning

confidence: 99%

Differential alterations of intracellular [Ca2+] dynamics induced by cocaine and methylphenidate in thalamocortical ventrobasal neurons

Rozas

Goitia

Bisagno

et al. 2017

Transl Brain Rhythmicity

View full text Add to dashboard Cite

The ventrobasal (VB) thalamus relay nucleus processes information from rodents’ whiskers, projecting to somatosensory cortex. Cocaine and methylphenidate (MPH) have been described to differentially alter intrinsic properties of, and spontaneous GABAergic input to, VB neurons. Here we studied using bis-fura 2 ratiometric fluorescence the effects of cocaine and MPH on intracellular [Ca2+] dynamics at the soma and dendrites of VB neurons. Cocaine increased baseline fluorescence in VB somatic and dendritic compartments. Peak and areas of fluorescence amplitudes were reduced by cocaine binge treatment in somas and dendrites at different holding potentials. MPH binge treatment did not alter ratiometric fluorescence at either somatic or dendritic levels. These novel cocaine-mediated blunting effects on intracellular [Ca2+] might account for alterations in the capacity of thalamocortical neurons to maintain gamma band oscillations, as well as their ability to integrate synaptic afferents.

show abstract

State-Dependent Firing Determines Intrinsic Dendritic Ca²⁺Signaling in Thalamocortical Neurons

Cited by 38 publications

References 45 publications

Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons

Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons

Characterization of Rebound Depolarization in Neurons of the Rat Medial Geniculate Body In Vitro

Differential alterations of intracellular [Ca2+] dynamics induced by cocaine and methylphenidate in thalamocortical ventrobasal neurons

Contact Info

Product

Resources

About

State-Dependent Firing Determines Intrinsic Dendritic Ca2+Signaling in Thalamocortical Neurons

Cited by 38 publications

References 45 publications

Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons

Variable Action Potential Backpropagation during Tonic Firing and Low-Threshold Spike Bursts in Thalamocortical But Not Thalamic Reticular Nucleus Neurons

Characterization of Rebound Depolarization in Neurons of the Rat Medial Geniculate Body In Vitro

Differential alterations of intracellular [Ca2+] dynamics induced by cocaine and methylphenidate in thalamocortical ventrobasal neurons

Contact Info

Product

Resources

About

State-Dependent Firing Determines Intrinsic Dendritic Ca²⁺Signaling in Thalamocortical Neurons