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Control of Xenopus tadpole locomotion via selective expression of Ih in excitatory interneurons

Research output: Contribution to journalArticle

Author(s)

Laurence D. Picton, Keith T. Sillar, Hong-Yan Zhang

School/Research organisations

Abstract

Locomotion relies on the coordinated activity of rhythmic neurons in the hindbrain and spinal cord, and depends critically on the intrinsic properties of excitatory interneurons. Therefore, understanding how ion channels sculpt the properties of these interneurons, and the consequences for circuit function and behavior, is an important task. The hyperpolarisation-activated cation current, Ih, is known to play important roles in shaping neuronal properties and for rhythm generation in many neuronal networks. We show in stage 42 Xenopus laevis frog tadpoles that Ih is strongly expressed only in excitatory descending interneurons (dINs), an important ipsilaterally-projecting population that drives swimming activity. The voltage-dependent HCN channel blocker ZD7288 completely abolished a prominent depolarising sag potential in response to hyperpolarisation, the hallmark of Ih, and hyperpolarised dINs. ZD7288 also affected dIN post-inhibitory rebound firing, upon which locomotor rhythm generation relies, and disrupted locomotor output. Block of Ih also unmasked an activity-dependent ultraslow afterhyperpolarisation (usAHP) in dINs following swimming, mediated by a dynamic Na/K pump current. This usAHP, unmasked in dINs by ZD7288, resulted in suprathreshold stimuli failing to evoke swimming at short inter-swim intervals, indicating an important role for Ih in maintaining swim generation capacity and in setting the post-swim refractory period of the network. Collectively, our data suggest that the selective expression of Ih in dINs determines specific dIN properties that are important for rhythm generation and counteracts an activity- dependent usAHP to ensure that dINs can maintain coordinated swimming over a wide range of inter-swim intervals.
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Details

Original languageEnglish
Pages (from-to)3911-3923
Number of pages16
JournalCurrent Biology
Volume28
Issue number24
Early online date29 Nov 2018
DOIs
Publication statusPublished - 17 Dec 2018

    Research areas

  • lh, HCN channels, Afterhyperpolarisation, Na/K pump, Xenopus, Central Pattern Generator

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