Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons

Tadayonnejad, Reza; Mehaffey, W. Hamish; Anderson, Dustin; Turner, Ray W.

doi:10.4161/chan.3.3.8872

Cited by 28 publications

(35 citation statements)

References 28 publications

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“…Previous studies on the cellular mechanisms underlying rebound capabilities have revealed that specific subtypes of the T-type Ca 2+ -channels mediate transient (Ca V 3.1) and weak (Ca V 3.3) rebound responses (19)(20)(21)58). Although our experiments did not identify whether the recorded neurons expressed each of these Ca V 3-subtypes, 3 of 27 CN neurons recorded in the awake mice showed considerably larger increases in their firing rates than others, which might implicate that these neurons express Ca V 3.1 T-type Ca 2+ -channels.…”

Section: Discussionmentioning

confidence: 99%

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Hoebeek

Witter

Ruigrok

et al. 2010

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

135

145

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The output of the cerebellar cortex is controlled by two main inputs, (i.e., the climbing fiber and mossy fiber-parallel fiber pathway) and activations of these inputs elicit characteristic effects in its Purkinje cells: that is, the so-called complex spikes and simple spikes. Target neurons of the Purkinje cells in the cerebellar nuclei show rebound firing, which has been implicated in the processing and storage of motor coordination signals. Yet, it is not known to what extent these rebound phenomena depend on different modes of Purkinje cell activation. Using extracellular as well as patch-clamp recordings, we show here in both anesthetized and awake rodents that simple and complex spike-like train stimuli to the cerebellar cortex, as well as direct activation of the inferior olive, all result in rebound increases of the firing frequencies of cerebellar nuclei neurons for up to 250 ms, whereas single-pulse stimuli to the cerebellar cortex predominantly elicit well-timed spiking activity without changing the firing frequency of cerebellar nuclei neurons. We conclude that the rebound phenomenon offers a rich and powerful mechanism for cerebellar nuclei neurons, which should allow them to differentially process the climbing fiber and mossy fiber inputs in a physiologically operating cerebellum.olivo-cerebellar loop | rebound firing | Purkinje cell | complex spikes | simple spikes N eurons in the cerebellar nuclei (CN) form the main output of the cerebellum (1). They include GABAergic neurons that provide an inhibitory feedback to the inferior olive (IO) and excitatory neurons that project to various other brainstem nuclei exerting motor control (2-4). In turn, each CN neuron receives a prominent inhibitory GABAergic input from tens of Purkinje cells, a substantial excitatory input from climbing fiber and mossy fiber collaterals, and a modest input from the local interneurons (4-7). Apart from the impact of these inputs, the firing pattern of CN neurons is largely determined by their intrinsic activities (4,(8)(9)(10)(11)(12)(13)(14). Interestingly, following inhibitory current injections or activation of their Purkinje cell input, CN neurons can show a "rebound" depolarization of the membrane potential, accompanied by action-potential firing (8, 11). Even though little is known about the prominence of rebound firing in the awake state, various models on cerebellar function consider this rebound phenomenon in the nuclei as an essential mechanism to process and store relevant information on motor coordination (15-18). The conductances that allow the rebound firing to emerge involve various types of Ca 2+ -channels, the distribution of which probably varies among the different types of neurons in the CN (8,11,14,(19)(20)(21)(22)(23). Regardless of the type of CN neuron, it is tempting to hypothesize that the climbing fibers and parallel fibers, which evoke complex spikes and simple spikes (24-27), respectively, have a differential impact on the generation of rebound activities in the CN neurons.To test this hypothe...

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Section: Discussionmentioning

confidence: 99%

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Hoebeek

Witter

Ruigrok

et al. 2010

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

135

145

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“…RE has been found in many different neuronal types and is postulated to participate in many functions and brain processes under normal and pathological conditions (Perez-Reyes 2003). Notable examples include the prominent RE of thalamic neurons thought to contribute to sleep and epilepsy (Andersen et al 1964;Kim et al 2001;Steriade and Llinás 1988), the RE found in neurons of circuits generating rhythmic motor outputs (Bertrand and Cazalets 1998;Miller and Selverston 1982;Syed et al 1990), the RE found in neurons of the olfactory and visual pathways (Balu and Strowbridge 2007;Liu and Shipley 2008;Lo et al 1998;Margolis et al 2010), the RE found in the GABAergic periaqueductal gray neurons involved in analgesia (Park et al 2010), and the RE described in neurons of the inferior olive and deep cerebellar nuclei (Aizenman and Linden 1999;Czubayko et al 2001;Jahnsen 1986a;Llinás and Mühlethaler 1988;Llinás and Yarom 1981;Molineux et al 2006;Pedroarena 2010;Pugh and Raman 2006;Tadayonnejad et al 2009;Uusisaari et al 2007) thought important for motor control and other aspects of cerebellar function.…”

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confidence: 99%

“…First, although RE can be evoked by inhibitory postsynaptic potentials (IPSPs) in DCNs in vitro (Llinás and Mühlethaler 1988;Aizenman et al 1998;Aizenman and Linden 1999;Pedroarena 2010;Sangrey and Jaeger 2010;Tadayonnejad et al 2009;Zheng and Raman 2009) and in vivo preparations (Hoebeek et al 2010), the limited hyperpolarization attained by chloride-dependent IPSPs has been noted as an obstacle for the deinactivation of T-type channels in DCNs Zheng and Raman 2009). Indeed, this issue applies to all neurons where the deinactivation of T-type calcium channels is expected to occur as a result of chloride-dependent inhibition.…”

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confidence: 99%

Rebound excitation triggered by synaptic inhibition in cerebellar nuclear neurons is suppressed by selective T-type calcium channel block

Boehme

Uebele

Renger

et al. 2011

Journal of Neurophysiology

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Following hyperpolarizing inputs, many neurons respond with an increase in firing rate, a phenomenon known as rebound excitation. Rebound excitation has been proposed as a mechanism to encode and process inhibitory signals and transfer them to target structures. Activation of low-voltage-activated T-type calcium channels and the ensuing low-threshold calcium spikes is one of the mechanisms proposed to support rebound excitation. However, there is still not enough evidence that the hyperpolarization provided by inhibitory inputs, particularly those dependent on chloride ions, is adequate to deinactivate a sufficient number of T-type calcium channels to drive rebound excitation on return to baseline. Here, this issue was investigated in the deep cerebellar nuclear neurons (DCNs), which receive the output of the cerebellar cortex conveyed exclusively by the inhibitory Purkinje cells and are also known to display rebound excitation. Using cerebellar slices and whole cell recordings of large DCNs, we show that a novel piperidine-based compound that selectively antagonizes T-type calcium channel activity, 3,5-dichloro-N-[1-(2,2-dimethyl-tetrahydropyran-4-ylmethyl)-4-fluoro-piperidin-4-ylmethyl]-benzamide (TTA-P2), suppressed rebound excitation elicited by current injection as well as by synaptic inhibition, whereas other electrophysiological properties of large DCNs were unaltered. Furthermore, TTA-P2 suppressed transient high-frequency rebounds found in DCNs with low-threshold spikes as well as the slow rebounds present in DCNs without low-threshold spikes. These findings demonstrate that chloride-dependent synaptic inhibition effectively triggers T-type calcium channel-mediated rebounds and that the latter channels may support slow rebound excitation in neurons without low-threshold spikes.

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“…Prior literature is not consistent on the prevalence of bursting neurons. In lateral and interpositus nuclei, few large cells are reported to burst (Zheng and Raman 2009), yet the interpositus is also reported to be a location in which TBs are abundant (Engbers et al 2011;Tadayonnejad et al 2009). We observed that burst firing depended on the amount of time animals were housed before slice preparation.…”

Section: Resultsmentioning

confidence: 99%

Calcium-based dendritic excitability and its regulation in the deep cerebellar nuclei

Schneider

Civillico

Wang

2013

Journal of Neurophysiology

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Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons

Cited by 28 publications

References 28 publications

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

Rebound excitation triggered by synaptic inhibition in cerebellar nuclear neurons is suppressed by selective T-type calcium channel block

Calcium-based dendritic excitability and its regulation in the deep cerebellar nuclei

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