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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

Colour-signals control irradiance coding in suprachiasmatic neurons.(A) Stimuli used to examine twilight coding: top panel indicates natural change in effective photon flux for each mouse opsin as a function of solar angle (0° represents sunrise/sunset), indicated points were recreated using a three-primary LED system. Note: values for LWS opsin stimulation were chosen to replicate those calculated for the wild-type MWS opsin under natural conditions. Bottom panels indicate control stimuli, which replicated the “natural” change in irradiance but lacked changes in colour (UVS opsin excitation held at a constant ratio relative to LWS, to mimic “day” or “night” spectra). (B) Mean (±SEM) normalised responses of blue-ON cells (n = 9) to 30-s light steps recreating the indicated stages of twilight. Responses were normalised on a within-cell basis according to the largest response observed across all three stimulus sets. (C) Initial (0–10 s) responses of cells from B as a function of simulated solar angle, fit with four-parameter sigmoid curves. Note influence of twilight spectral composition on the solar angle response curve (F-test for difference in curve parameters; p = 0.009; direct comparisons between each pair of curves also revealed significant differences p<0.05). (D and E) Responses of achromatic cells (n = 8), conventions as in B and C. Achromatic cell responses to the three stimulus sets were statistically indistinguishable (F-test; p = 0.72). The data used to make this figure can be found in S4 Data.
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pbio.1002127.g004: Colour-signals control irradiance coding in suprachiasmatic neurons.(A) Stimuli used to examine twilight coding: top panel indicates natural change in effective photon flux for each mouse opsin as a function of solar angle (0° represents sunrise/sunset), indicated points were recreated using a three-primary LED system. Note: values for LWS opsin stimulation were chosen to replicate those calculated for the wild-type MWS opsin under natural conditions. Bottom panels indicate control stimuli, which replicated the “natural” change in irradiance but lacked changes in colour (UVS opsin excitation held at a constant ratio relative to LWS, to mimic “day” or “night” spectra). (B) Mean (±SEM) normalised responses of blue-ON cells (n = 9) to 30-s light steps recreating the indicated stages of twilight. Responses were normalised on a within-cell basis according to the largest response observed across all three stimulus sets. (C) Initial (0–10 s) responses of cells from B as a function of simulated solar angle, fit with four-parameter sigmoid curves. Note influence of twilight spectral composition on the solar angle response curve (F-test for difference in curve parameters; p = 0.009; direct comparisons between each pair of curves also revealed significant differences p<0.05). (D and E) Responses of achromatic cells (n = 8), conventions as in B and C. Achromatic cell responses to the three stimulus sets were statistically indistinguishable (F-test; p = 0.72). The data used to make this figure can be found in S4 Data.

Mentions: How then do chromatic and irradiance responses interact to encode time of day under more natural conditions? To address this question, we produced stimuli that recreated, for Opn1mwR mice, the change in irradiance and colour experienced by wild-type (green cone) mice across the twilight to daylight transition (Fig 4A). We presented these as discrete light steps from darkness, to simulate the challenge in telling time of day faced by a rodent emerging from a subterranean burrow to sample the light environment. Due to their scarcity, we were unable to determine the behaviour of yellow-ON cells under these conditions. However, blue ON cells reliably exhibited a near linear increase in firing rate as a function of simulated solar angle (Fig 4B and 4C; n = 9 from 7 mice), indicating that their sensitivity is well suited to track changes in colour/irradiance occurring across the twilight to daylight transition. Interestingly, the range of solar angles to which these neurons responded was substantially greater than that for achromatic cells recorded in the same set of mice (Fig 4D and 4E; see also S3 Fig; n = 8) indicating that they may be an especially important source of temporal information for the clock around twilight.


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)

Colour-signals control irradiance coding in suprachiasmatic neurons.(A) Stimuli used to examine twilight coding: top panel indicates natural change in effective photon flux for each mouse opsin as a function of solar angle (0° represents sunrise/sunset), indicated points were recreated using a three-primary LED system. Note: values for LWS opsin stimulation were chosen to replicate those calculated for the wild-type MWS opsin under natural conditions. Bottom panels indicate control stimuli, which replicated the “natural” change in irradiance but lacked changes in colour (UVS opsin excitation held at a constant ratio relative to LWS, to mimic “day” or “night” spectra). (B) Mean (±SEM) normalised responses of blue-ON cells (n = 9) to 30-s light steps recreating the indicated stages of twilight. Responses were normalised on a within-cell basis according to the largest response observed across all three stimulus sets. (C) Initial (0–10 s) responses of cells from B as a function of simulated solar angle, fit with four-parameter sigmoid curves. Note influence of twilight spectral composition on the solar angle response curve (F-test for difference in curve parameters; p = 0.009; direct comparisons between each pair of curves also revealed significant differences p<0.05). (D and E) Responses of achromatic cells (n = 8), conventions as in B and C. Achromatic cell responses to the three stimulus sets were statistically indistinguishable (F-test; p = 0.72). The data used to make this figure can be found in S4 Data.
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Related In: Results  -  Collection

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

pbio.1002127.g004: Colour-signals control irradiance coding in suprachiasmatic neurons.(A) Stimuli used to examine twilight coding: top panel indicates natural change in effective photon flux for each mouse opsin as a function of solar angle (0° represents sunrise/sunset), indicated points were recreated using a three-primary LED system. Note: values for LWS opsin stimulation were chosen to replicate those calculated for the wild-type MWS opsin under natural conditions. Bottom panels indicate control stimuli, which replicated the “natural” change in irradiance but lacked changes in colour (UVS opsin excitation held at a constant ratio relative to LWS, to mimic “day” or “night” spectra). (B) Mean (±SEM) normalised responses of blue-ON cells (n = 9) to 30-s light steps recreating the indicated stages of twilight. Responses were normalised on a within-cell basis according to the largest response observed across all three stimulus sets. (C) Initial (0–10 s) responses of cells from B as a function of simulated solar angle, fit with four-parameter sigmoid curves. Note influence of twilight spectral composition on the solar angle response curve (F-test for difference in curve parameters; p = 0.009; direct comparisons between each pair of curves also revealed significant differences p<0.05). (D and E) Responses of achromatic cells (n = 8), conventions as in B and C. Achromatic cell responses to the three stimulus sets were statistically indistinguishable (F-test; p = 0.72). The data used to make this figure can be found in S4 Data.
Mentions: How then do chromatic and irradiance responses interact to encode time of day under more natural conditions? To address this question, we produced stimuli that recreated, for Opn1mwR mice, the change in irradiance and colour experienced by wild-type (green cone) mice across the twilight to daylight transition (Fig 4A). We presented these as discrete light steps from darkness, to simulate the challenge in telling time of day faced by a rodent emerging from a subterranean burrow to sample the light environment. Due to their scarcity, we were unable to determine the behaviour of yellow-ON cells under these conditions. However, blue ON cells reliably exhibited a near linear increase in firing rate as a function of simulated solar angle (Fig 4B and 4C; n = 9 from 7 mice), indicating that their sensitivity is well suited to track changes in colour/irradiance occurring across the twilight to daylight transition. Interestingly, the range of solar angles to which these neurons responded was substantially greater than that for achromatic cells recorded in the same set of mice (Fig 4D and 4E; see also S3 Fig; n = 8) indicating that they may be an especially important source of temporal information for the clock around twilight.

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