Literature DB >> 30044671

M current regulates firing mode and spike reliability in a collision-detecting neuron.

Richard B Dewell1, Fabrizio Gabbiani1,2.   

Abstract

All animals must detect impending collisions to escape and reliably discriminate them from nonthreatening stimuli, thus preventing false alarms. Therefore, it is no surprise that animals have evolved highly selective and sensitive neurons dedicated to such tasks. We examined a well-studied collision-detection neuron in the grasshopper ( Schistocerca americana) using in vivo electrophysiology, pharmacology, and computational modeling. This lobula giant movement detector (LGMD) neuron is excitable by inputs originating from each ommatidia of the compound eye. It possesses many intrinsic properties that increase its selectivity to objects approaching on a collision course, including switching between burst and nonburst firing. In this study, we demonstrate that the LGMD neuron exhibits a large M current, generated by noninactivating K+ channels, that shortens the temporal window of dendritic integration, regulates a firing mode switch between burst and isolated spiking, increases the precision of spike timing, and increases the reliability of spike propagation to downstream motor centers. By revealing how the M current increases the LGMD's ability to detect impending collisions, our results suggest that similar channels may play an analogous role in other collision detection circuits. NEW & NOTEWORTHY The ability to reliably detect impending collisions is a critical survival skill. The nervous systems of many animals have developed dedicated neurons for accomplishing this task. We used a mix of in vivo electrophysiology and computational modeling to investigate the role of M potassium channels within one such collision-detecting neuron and show that through regulation of burst firing and enhancement of spiking reliability, the M current increases the ability to detect impending collisions.

Entities:  

Keywords:  M current; burst firing; collision avoidance; lobula giant movement detector; spike timing

Mesh:

Substances:

Year:  2018        PMID: 30044671      PMCID: PMC6230786          DOI: 10.1152/jn.00363.2018

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  57 in total

1.  Activity of descending contralateral movement detector neurons and collision avoidance behaviour in response to head-on visual stimuli in locusts.

Authors:  J R Gray; J K Lee; R M Robertson
Journal:  J Comp Physiol A       Date:  2001-03       Impact factor: 1.836

Review 2.  Pathways modulating neural KCNQ/M (Kv7) potassium channels.

Authors:  Patrick Delmas; David A Brown
Journal:  Nat Rev Neurosci       Date:  2005-11       Impact factor: 34.870

3.  Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release.

Authors:  K Vervaeke; N Gu; C Agdestein; H Hu; J F Storm
Journal:  J Physiol       Date:  2006-07-13       Impact factor: 5.182

4.  HCN channels enhance spike phase coherence and regulate the phase of spikes and LFPs in the theta-frequency range.

Authors:  Manisha Sinha; Rishikesh Narayanan
Journal:  Proc Natl Acad Sci U S A       Date:  2015-04-13       Impact factor: 11.205

5.  M-type potassium conductance controls the emergence of neural phase codes: a combined experimental and neuron modelling study.

Authors:  Jeehyun Kwag; Hyun Jae Jang; Mincheol Kim; Sujeong Lee
Journal:  J R Soc Interface       Date:  2014-10-06       Impact factor: 4.118

6.  Task-specific sensory coding strategies are matched to detection and discrimination performance.

Authors:  Kathryne M Allen; Gary Marsat
Journal:  J Exp Biol       Date:  2018-03-27       Impact factor: 3.312

7.  Low-conductance HCN1 ion channels augment the frequency response of rod and cone photoreceptors.

Authors:  Andrew J Barrow; Samuel M Wu
Journal:  J Neurosci       Date:  2009-05-06       Impact factor: 6.167

8.  KCNQ channels mediate IKs, a slow K+ current regulating excitability in the rat node of Ranvier.

Authors:  J R Schwarz; G Glassmeier; E C Cooper; T-C Kao; H Nodera; D Tabuena; R Kaji; H Bostock
Journal:  J Physiol       Date:  2006-03-09       Impact factor: 5.182

9.  Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron.

Authors:  Simon Peron; Fabrizio Gabbiani
Journal:  Nat Neurosci       Date:  2009-02-08       Impact factor: 24.884

10.  Differential effects of Kv7 (M-) channels on synaptic integration in distinct subcellular compartments of rat hippocampal pyramidal neurons.

Authors:  Mala M Shah; Michele Migliore; David A Brown
Journal:  J Physiol       Date:  2011-10-31       Impact factor: 5.182

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  3 in total

1.  Active membrane conductances and morphology of a collision detection neuron broaden its impedance profile and improve discrimination of input synchrony.

Authors:  Richard B Dewell; Fabrizio Gabbiani
Journal:  J Neurophysiol       Date:  2019-07-03       Impact factor: 2.714

2.  A model of feedforward, global, and lateral inhibition in the locust visual system predicts responses to looming stimuli.

Authors:  Erik G N Olson; Travis K Wiens; John R Gray
Journal:  Biol Cybern       Date:  2021-05-16       Impact factor: 2.086

3.  Impaired Reliability and Precision of Spiking in Adults But Not Juveniles in a Mouse Model of Fragile X Syndrome.

Authors:  Deepanjali Dwivedi; Sumantra Chattarji; Upinder S Bhalla
Journal:  eNeuro       Date:  2019-12-03
  3 in total

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