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Colour as a signal for entraining the mammalian circadian clock.

Walmsley L, Hanna L, Mouland J, Martial F, West A, Smedley AR, Bechtold DA, Webb AR, Lucas RJ, Brown TM - PLoS Biol. (2015)

Bottom Line: Thus, our data show that some clock neurons are highly sensitive to changes in spectral composition occurring over twilight and that this input dictates their response to changes in irradiance.Finally, using mice housed under photoperiods with simulated dawn/dusk transitions, we confirm that spectral changes occurring during twilight are required for appropriate circadian alignment under natural conditions.Together, these data reveal a new sensory mechanism for telling time of day that would be available to any mammalian species capable of chromatic vision.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.

ABSTRACT
Twilight is characterised by changes in both quantity ("irradiance") and quality ("colour") of light. Animals use the variation in irradiance to adjust their internal circadian clocks, aligning their behaviour and physiology with the solar cycle. However, it is currently unknown whether changes in colour also contribute to this entrainment process. Using environmental measurements, we show here that mammalian blue-yellow colour discrimination provides a more reliable method of tracking twilight progression than simply measuring irradiance. We next use electrophysiological recordings to demonstrate that neurons in the mouse suprachiasmatic circadian clock display the cone-dependent spectral opponency required to make use of this information. Thus, our data show that some clock neurons are highly sensitive to changes in spectral composition occurring over twilight and that this input dictates their response to changes in irradiance. Finally, using mice housed under photoperiods with simulated dawn/dusk transitions, we confirm that spectral changes occurring during twilight are required for appropriate circadian alignment under natural conditions. Together, these data reveal a new sensory mechanism for telling time of day that would be available to any mammalian species capable of chromatic vision.

No MeSH data available.


Related in: MedlinePlus

Twilight spectral composition regulates photoperiodic encoding in the suprachiasmatic nuclei.(A–B) Phasing of SCN firing rhythms from ex vivo multielectrode array recordings of Opn1mwR mice housed under natural (A) or irradiance-only (B) twilight photoperiods. Left panels show Rayleigh vector plots for peak firing activity (n = 124 and 170 SCN electrodes from seven and six slices in A and B respectively). Grey-shaded areas correspond to timing of night/twilight transitions, red dotted lines indicate central 50% of the data distribution, arrows indicate mean vector direction. Right panels show representative multiunit traces. Consistent with body temperature data (Fig 5), SCN activity peaks later in mice housed under “natural” relative to irradiance-only twilight (p<0.001 based on bootstrap percentiles). The data used to make this figure can be found in S6 Data.
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pbio.1002127.g006: Twilight spectral composition regulates photoperiodic encoding in the suprachiasmatic nuclei.(A–B) Phasing of SCN firing rhythms from ex vivo multielectrode array recordings of Opn1mwR mice housed under natural (A) or irradiance-only (B) twilight photoperiods. Left panels show Rayleigh vector plots for peak firing activity (n = 124 and 170 SCN electrodes from seven and six slices in A and B respectively). Grey-shaded areas correspond to timing of night/twilight transitions, red dotted lines indicate central 50% of the data distribution, arrows indicate mean vector direction. Right panels show representative multiunit traces. Consistent with body temperature data (Fig 5), SCN activity peaks later in mice housed under “natural” relative to irradiance-only twilight (p<0.001 based on bootstrap percentiles). The data used to make this figure can be found in S6 Data.

Mentions: As further confirmation that these differences in body temperature cycles reflected an action on the timing of central clock output, we also monitored SCN firing rate rhythms in a subset of mice via ex vivo multielectrode array recordings. We and others have previously shown that the distribution of daily electrical activity patterns among individual SCN neurons encodes photoperiod duration, resulting in broad phase distributions under summer days [31,32]. Consistent with this work, peak multiunit firing (sampled across small groups of neurons) in the ex vivo SCN of twilight-housed mice was widely distributed across recording epochs corresponding to projected day. Importantly, in line with our body temperature data, this distribution was centred around the middle of the projected day for Opn1mwR mice exposed to “natural” twilight (Fig 6A; n = 124 SCN electrodes from seven slices) but shifted substantially earlier when mice were housed under twilight that lacked changes in colour (Fig 6B; p<0.001, bootstrap percentiles; n = 170 SCN electrodes from six slices). A similarly early phase of peak SCN electrical activity was also observed in slices prepared from Cnga3-/- individuals housed under natural twilight (S5 Fig; p<0.001 versus Opn1mwR, bootstrap percentiles), confirming that the cone-dependent colour signal is indeed required for appropriate biological alignment with twilight. We also found that, across the three groups, Opn1mwR mice exposed to “irradiance-only” twilight exhibited a significantly broader distribution of SCN phasing (Brown-Forsythe test, p = 0.01), suggesting that the inappropriate cone signals under this photoperiod partially impair SCN synchrony.


Colour as a signal for entraining the mammalian circadian clock.

Walmsley L, Hanna L, Mouland J, Martial F, West A, Smedley AR, Bechtold DA, Webb AR, Lucas RJ, Brown TM - PLoS Biol. (2015)

Twilight spectral composition regulates photoperiodic encoding in the suprachiasmatic nuclei.(A–B) Phasing of SCN firing rhythms from ex vivo multielectrode array recordings of Opn1mwR mice housed under natural (A) or irradiance-only (B) twilight photoperiods. Left panels show Rayleigh vector plots for peak firing activity (n = 124 and 170 SCN electrodes from seven and six slices in A and B respectively). Grey-shaded areas correspond to timing of night/twilight transitions, red dotted lines indicate central 50% of the data distribution, arrows indicate mean vector direction. Right panels show representative multiunit traces. Consistent with body temperature data (Fig 5), SCN activity peaks later in mice housed under “natural” relative to irradiance-only twilight (p<0.001 based on bootstrap percentiles). The data used to make this figure can be found in S6 Data.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4401556&req=5

pbio.1002127.g006: Twilight spectral composition regulates photoperiodic encoding in the suprachiasmatic nuclei.(A–B) Phasing of SCN firing rhythms from ex vivo multielectrode array recordings of Opn1mwR mice housed under natural (A) or irradiance-only (B) twilight photoperiods. Left panels show Rayleigh vector plots for peak firing activity (n = 124 and 170 SCN electrodes from seven and six slices in A and B respectively). Grey-shaded areas correspond to timing of night/twilight transitions, red dotted lines indicate central 50% of the data distribution, arrows indicate mean vector direction. Right panels show representative multiunit traces. Consistent with body temperature data (Fig 5), SCN activity peaks later in mice housed under “natural” relative to irradiance-only twilight (p<0.001 based on bootstrap percentiles). The data used to make this figure can be found in S6 Data.
Mentions: As further confirmation that these differences in body temperature cycles reflected an action on the timing of central clock output, we also monitored SCN firing rate rhythms in a subset of mice via ex vivo multielectrode array recordings. We and others have previously shown that the distribution of daily electrical activity patterns among individual SCN neurons encodes photoperiod duration, resulting in broad phase distributions under summer days [31,32]. Consistent with this work, peak multiunit firing (sampled across small groups of neurons) in the ex vivo SCN of twilight-housed mice was widely distributed across recording epochs corresponding to projected day. Importantly, in line with our body temperature data, this distribution was centred around the middle of the projected day for Opn1mwR mice exposed to “natural” twilight (Fig 6A; n = 124 SCN electrodes from seven slices) but shifted substantially earlier when mice were housed under twilight that lacked changes in colour (Fig 6B; p<0.001, bootstrap percentiles; n = 170 SCN electrodes from six slices). A similarly early phase of peak SCN electrical activity was also observed in slices prepared from Cnga3-/- individuals housed under natural twilight (S5 Fig; p<0.001 versus Opn1mwR, bootstrap percentiles), confirming that the cone-dependent colour signal is indeed required for appropriate biological alignment with twilight. We also found that, across the three groups, Opn1mwR mice exposed to “irradiance-only” twilight exhibited a significantly broader distribution of SCN phasing (Brown-Forsythe test, p = 0.01), suggesting that the inappropriate cone signals under this photoperiod partially impair SCN synchrony.

Bottom Line: Thus, our data show that some clock neurons are highly sensitive to changes in spectral composition occurring over twilight and that this input dictates their response to changes in irradiance.Finally, using mice housed under photoperiods with simulated dawn/dusk transitions, we confirm that spectral changes occurring during twilight are required for appropriate circadian alignment under natural conditions.Together, these data reveal a new sensory mechanism for telling time of day that would be available to any mammalian species capable of chromatic vision.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom.

ABSTRACT
Twilight is characterised by changes in both quantity ("irradiance") and quality ("colour") of light. Animals use the variation in irradiance to adjust their internal circadian clocks, aligning their behaviour and physiology with the solar cycle. However, it is currently unknown whether changes in colour also contribute to this entrainment process. Using environmental measurements, we show here that mammalian blue-yellow colour discrimination provides a more reliable method of tracking twilight progression than simply measuring irradiance. We next use electrophysiological recordings to demonstrate that neurons in the mouse suprachiasmatic circadian clock display the cone-dependent spectral opponency required to make use of this information. Thus, our data show that some clock neurons are highly sensitive to changes in spectral composition occurring over twilight and that this input dictates their response to changes in irradiance. Finally, using mice housed under photoperiods with simulated dawn/dusk transitions, we confirm that spectral changes occurring during twilight are required for appropriate circadian alignment under natural conditions. Together, these data reveal a new sensory mechanism for telling time of day that would be available to any mammalian species capable of chromatic vision.

No MeSH data available.


Related in: MedlinePlus