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Cover ArticleFeatured ArticleResearch Articles, Cellular/Molecular

Cone-Driven Retinal Responses Are Shaped by Rod But Not Cone HCN1

Colten K. Lankford, Yumiko Umino, Deepak Poria, Vladimir Kefalov, Eduardo Solessio and Sheila A. Baker
Journal of Neuroscience 25 May 2022, 42 (21) 4231-4249; DOI: https://doi.org/10.1523/JNEUROSCI.2271-21.2022
Colten K. Lankford
1Department of Biochemistry and Molecular Biology, University of Iowa, Iowa City, Iowa 52242
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Yumiko Umino
2Center for Vision Research, Department of Ophthalmology and Visual Sciences, State University of New York Upstate Medical University, Syracuse, New York 13210
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Deepak Poria
3Department of Ophthalmology, Gavin Herbert Eye Institute, University of California, Irvine, California 92697
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Vladimir Kefalov
3Department of Ophthalmology, Gavin Herbert Eye Institute, University of California, Irvine, California 92697
4Department of Physiology and Biophysics, University of California, Irvine, California 92697
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Eduardo Solessio
2Center for Vision Research, Department of Ophthalmology and Visual Sciences, State University of New York Upstate Medical University, Syracuse, New York 13210
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Sheila A. Baker
1Department of Biochemistry and Molecular Biology, University of Iowa, Iowa City, Iowa 52242
5Department of Ophthalmology and Visual Sciences and Institute for Vision Research, University of Iowa, Iowa City, Iowa 52242
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Abstract

Signal integration of converging neural circuits is poorly understood. One example is in the retina where the integration of rod and cone signaling is responsible for the large dynamic range of vision. The relative contribution of rods versus cones is dictated by a complex function involving background light intensity and stimulus temporal frequency. One understudied mechanism involved in coordinating rod and cone signaling onto the shared retinal circuit is the hyperpolarization activated current (Ih) mediated by hyperpolarization-activated cyclic nucleotide-gated 1 (HCN1) channels expressed in rods and cones. Ih opposes membrane hyperpolarization driven by activation of the phototransduction cascade and modulates the strength and kinetics of the photoreceptor voltage response. We examined conditional knock-out (KO) of HCN1 from mouse rods using electroretinography (ERG). In the absence of HCN1, rod responses are prolonged in dim light which altered the response to slow modulation of light intensity both at the level of retinal signaling and behavior. Under brighter intensities, cone-driven signaling was suppressed. To our surprise, conditional KO of HCN1 from mouse cones had no effect on cone-mediated signaling. We propose that Ih is dispensable in cones because of the high level of temporal control of cone phototransduction. Thus, HCN1 is required for cone-driven retinal signaling only indirectly by modulating the voltage response of rods to limit their output.

SIGNIFICANCE STATEMENT Hyperpolarization gated hyperpolarization-activated cyclic nucleotide-gated 1 (HCN1) channels carry a feedback current that helps to reset light-activated photoreceptors. Using conditional HCN1 knock-out (KO) mice we show that ablating HCN1 from rods allows rods to signal in bright light when they are normally shut down. Instead of enhancing vision this results in suppressing cone signaling. Conversely, ablating HCN1 from cones was of no consequence. This work provides novel insights into the integration of rod and cone signaling in the retina and challenges our assumptions about the role of HCN1 in cones.

  • cone
  • ERG
  • HCN1
  • light adaptation
  • photovoltage
  • rod

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The Journal of Neuroscience: 42 (21)
Journal of Neuroscience
Vol. 42, Issue 21
25 May 2022
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Cone-Driven Retinal Responses Are Shaped by Rod But Not Cone HCN1
Colten K. Lankford, Yumiko Umino, Deepak Poria, Vladimir Kefalov, Eduardo Solessio, Sheila A. Baker
Journal of Neuroscience 25 May 2022, 42 (21) 4231-4249; DOI: 10.1523/JNEUROSCI.2271-21.2022

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Cone-Driven Retinal Responses Are Shaped by Rod But Not Cone HCN1
Colten K. Lankford, Yumiko Umino, Deepak Poria, Vladimir Kefalov, Eduardo Solessio, Sheila A. Baker
Journal of Neuroscience 25 May 2022, 42 (21) 4231-4249; DOI: 10.1523/JNEUROSCI.2271-21.2022
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Keywords

  • cone
  • ERG
  • HCN1
  • light adaptation
  • photovoltage
  • rod

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