Dataset Information

Balanced Activity between Kv3 and Nav Channels Determines Fast-Spiking in Mammalian Central Neurons.

ABSTRACT: Fast-spiking (FS) neurons can fire action potentials (APs) up to 1,000 Hz and play key roles in vital functions such as sound location, motor coordination, and cognition. Here we report that the concerted actions of Kv3 voltage-gated K+ (Kv) and Na+ (Nav) channels are sufficient and necessary for inducing and maintaining FS. Voltage-clamp analysis revealed a robust correlation between the Kv3/Nav current ratio and FS. Expressing Kv3 channels alone could convert ?30%-60% slow-spiking (SS) neurons to FS in culture. In contrast, co-expression of either Nav1.2 or Nav1.6 together with Kv3.1 or Kv3.3, but not alone or with Kv1.2, converted SS to FS with 100% efficiency. Furthermore, RNA-sequencing-based genome-wide analysis revealed that the Kv3/Nav ratio and Kv3 expression levels strongly correlated with the maximal AP frequencies. Therefore, FS is established by the properly balanced activities of Kv3 and Nav channels and could be further fine-tuned by channel biophysical features and localization patterns.

SUBMITTER: Gu Y

PROVIDER: S-EPMC6218699 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Publications

Balanced Activity between Kv3 and Nav Channels Determines Fast-Spiking in Mammalian Central Neurons.

Gu Yuanzheng Y Servello Dustin D Han Zhi Z Lalchandani Rupa R RR Ding Jun B JB Huang Kun K Gu Chen C

iScience 20181018

Fast-spiking (FS) neurons can fire action potentials (APs) up to 1,000 Hz and play key roles in vital functions such as sound location, motor coordination, and cognition. Here we report that the concerted actions of Kv3 voltage-gated K<sup>+</sup> (Kv) and Na<sup>+</sup> (Nav) channels are sufficient and necessary for inducing and maintaining FS. Voltage-clamp analysis revealed a robust correlation between the Kv3/Nav current ratio and FS. Expressing Kv3 channels alone could convert ∼30%-60% slo ...[more]

PMID: 30390433

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Project description:Background: Timing dysfunctions occur in a number of neurological and psychiatric disorders such as Parkinson's disease, obsessive-compulsive disorder, autism and attention-deficit-hyperactivity disorder. Several lines of evidence show that disrupted timing processing is involved in specific fronto-striatal abnormalities. The striatum encodes reinforcement learning and procedural motion, and consequently is required to represent temporal information precisely, which then guides actions in proper sequence. Previous studies highlighted the temporal scaling property of timing-relevant striatal neurons; however, it is still unknown how this is accomplished over short temporal latencies, such as the sub-seconds to seconds range. Methods: We designed a task with a series of timing behaviors that required rats to reproduce a fixed duration with robust action. Using chronic multichannel electrode arrays, we recorded neural activity from dorso-medial striatum in 4 rats performing the task and identified modulation response of each neuron to different events. Cell type classification was performed according to a multi-criteria clustering analysis. Results: Dorso-medial striatal neurons (n = 557) were recorded, of which 113 single units were considered as timing-relevant neurons, especially the fast-spiking subpopulation that had trial-to-trial ramping up or ramping down firing modulation during the time estimation period. Furthermore, these timing-relevant striatal neurons had to calibrate the spread of their firing pattern by rewarded experience to express the timing behavior accurately. Conclusion: Our data suggests that the dynamic activities of timing-relevant units encode information about the current duration and recent outcomes, which is needed to predict and drive the following action. These results reveal the potential mechanism of time calibration in a short temporal resolution, which may help to explain the neural basis of motor coordination affected by certain physiological or pathological conditions.

Dataset Information

Balanced Activity between Kv3 and Nav Channels Determines Fast-Spiking in Mammalian Central Neurons.

Publications

Balanced Activity between Kv3 and Nav Channels Determines Fast-Spiking in Mammalian Central Neurons.

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