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Mice Reach Higher Visual Sensitivity at Night by Using a More Efficient Behavioral Strategy

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Abstract

Circadian clocks predictively adjust the physiology of organisms to the day/night cycle. The retina has its own clock, and many diurnal changes in its physiology have been reported. However, their implications for retinal functions and visually guided behavior are largely unresolved. Here, we study the impact of diurnal rhythm on the sensitivity limit of mouse vision. A simple photon detection task allowed us to link well-defined retinal output signals directly to visually guided behavior. We show that visually guided behavior at its sensitivity limit is strongly under diurnal control, reaching the highest sensitivity and stability at night. The diurnal differences in visual sensitivity did not arise in the retina, as assessed by spike recordings from the most sensitive retinal ganglion cell types: ON sustained, OFF sustained, and OFF transient alpha ganglion cells. Instead, we found that mice, as nocturnal animals, use a more efficient search strategy for visual cues at night. Intriguingly, they can switch to the more efficient night strategy even at their subjective day after first having performed the task at night. Our results exemplify that the shape of visual psychometric functions depends robustly on the diurnal state of the animal, its search strategy, and even its diurnal history of performing the task. The results highlight the impact of the day/night cycle on high-level sensory processing, demonstrating a direct diurnal impact on the behavioral strategy of the animal.

Original languageEnglish
Article numbere4
Pages (from-to)42-53
Number of pages16
JournalCurrent Biology
Volume30
Issue number1
DOIs
Publication statusPublished - 6 Jan 2020
MoE publication typeA1 Journal article-refereed

Funding

We thank our lab manager, Mr. Sami Minkkinen, and Dr. Daisuke Takeshita in our lab for excellent technical assistance; Drs. Kristian Donner, Robert Lucas, Greg Schwartz, Anna St?ckl, Markku Kilpel?inen, and Johan West? for valuable comments on the manuscript; Matthew Dunkerley and Sathish Narayanan for the design of the data acquisition software. Support was provided by the Academy of Finland (253314, 256156, 283268, 296269, 305834 to P.A.-L.); the Sigrid Jus?lius Foundation (P.A.-L.); the Emil Aaltonen Foundation (P.A.-L.); the Doctoral programme Brain & Mind, University of Helsinki (S.K.); the Oskar ?flund Foundation (S.K.); the Otto A. Malm Foundation (S.K.); the Oskar ?flund Foundation, Finland; and the Ella and Georg Ehrnrooth Foundation (S.K. and T.T.). S.K. and P.A.-L. designed experiments; S.K. performed RGC and behavioral experiments; T.T. developed the methodology for tracking mice; and S.K. T.T. and P.A.-L. analyzed the data and wrote the manuscript. Patents related to ?A method for performing behavioral experiments with rodents? (T.T. and P.A.-L.): FI patent 2016105 and pending US patent application US15/493,161.

Keywords

  • animal tracking
  • arousal
  • behavior
  • brain state
  • circadian rhythm
  • ganglion cell
  • mouse
  • neural circuit
  • retina
  • vision

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