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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 opponent responses in suprachiasmatic neurons.(A: left) Example responses of 5 SCN neurons to stimuli modulating UVS and LWS opsin excitation in antiphase (“colour”) or in unison (“brightness”; both 70% Michelson contrast). Individual cells were preferentially excited by blue–yellow transitions (“blue ON”; pink traces), yellow-blue transitions (“yellow ON”; green traces) or dim-bright transitions (“achromatic”; black traces). Shaded areas represent blue/yellow or dim/bright stimulus phase; y-axis scale bars reflects peak firing rate in spikes/s; x-axis scale bars indicate temporal profile of UVS/LWS opsin excitation. (A: right) Normalised mean (±SEM) change in firing for cells classified as “blue-ON”, “yellow-ON” or achromatic (n = 13, 4 and 26 respectively). Conventions as above. (B) Mean (±SEM) firing rates of SCN cell populations tested with colour and brightness stimuli immediately following transitions (0–500 ms) from “blue”–”yellow”/”dim”–”bright” or vice versa. Data were analysed by paired t test; *** p<0.001, ** p<0.01. (C: left) Responses of cells from A to selective modulation of LWS or UVS opsin excitation, indicating “blue”-ON/”yellow-OFF”, “yellow-ON”/”blue-OFF” or non-opponent responses (conventions as in A). (C: right) Normalised mean (±SEM) change in firing for SCN cell populations evoked by LWS and UVS opsin isolating stimuli. Note, normalisation and scaling for data in A and C is identical. The data used to make this figure can be found in S2 Data.
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pbio.1002127.g002: Colour opponent responses in suprachiasmatic neurons.(A: left) Example responses of 5 SCN neurons to stimuli modulating UVS and LWS opsin excitation in antiphase (“colour”) or in unison (“brightness”; both 70% Michelson contrast). Individual cells were preferentially excited by blue–yellow transitions (“blue ON”; pink traces), yellow-blue transitions (“yellow ON”; green traces) or dim-bright transitions (“achromatic”; black traces). Shaded areas represent blue/yellow or dim/bright stimulus phase; y-axis scale bars reflects peak firing rate in spikes/s; x-axis scale bars indicate temporal profile of UVS/LWS opsin excitation. (A: right) Normalised mean (±SEM) change in firing for cells classified as “blue-ON”, “yellow-ON” or achromatic (n = 13, 4 and 26 respectively). Conventions as above. (B) Mean (±SEM) firing rates of SCN cell populations tested with colour and brightness stimuli immediately following transitions (0–500 ms) from “blue”–”yellow”/”dim”–”bright” or vice versa. Data were analysed by paired t test; *** p<0.001, ** p<0.01. (C: left) Responses of cells from A to selective modulation of LWS or UVS opsin excitation, indicating “blue”-ON/”yellow-OFF”, “yellow-ON”/”blue-OFF” or non-opponent responses (conventions as in A). (C: right) Normalised mean (±SEM) change in firing for SCN cell populations evoked by LWS and UVS opsin isolating stimuli. Note, normalisation and scaling for data in A and C is identical. The data used to make this figure can be found in S2 Data.

Mentions: To achieve the largest possible change in colour, we started by selectively modulating UVS and LWS cone opsin excitation in antiphase (“colour”; S1B Fig). We then compared responses to this stimulus with those elicited by one in which the change in UVS and LWS opsin activation occurred in unison (“brightness”; S1B Fig). Any spectrally opponent cells should be more responsive to the “colour” as opposed to “brightness” condition. We found that 17/43 SCN units (from 15 mice) that responded to these stimuli showed a significant preference for the pair in which UVS and LWS activation was modulated in antiphase (Fig 2A and 2B; paired t test, p<0.05, n = 17). As there were an additional 26 visually responsive units that did not respond to either of these analytical stimuli (paired t tests, p>0.05), these data indicate that at least one quarter of light-responsive SCN neurones show chromatic opponency.


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 opponent responses in suprachiasmatic neurons.(A: left) Example responses of 5 SCN neurons to stimuli modulating UVS and LWS opsin excitation in antiphase (“colour”) or in unison (“brightness”; both 70% Michelson contrast). Individual cells were preferentially excited by blue–yellow transitions (“blue ON”; pink traces), yellow-blue transitions (“yellow ON”; green traces) or dim-bright transitions (“achromatic”; black traces). Shaded areas represent blue/yellow or dim/bright stimulus phase; y-axis scale bars reflects peak firing rate in spikes/s; x-axis scale bars indicate temporal profile of UVS/LWS opsin excitation. (A: right) Normalised mean (±SEM) change in firing for cells classified as “blue-ON”, “yellow-ON” or achromatic (n = 13, 4 and 26 respectively). Conventions as above. (B) Mean (±SEM) firing rates of SCN cell populations tested with colour and brightness stimuli immediately following transitions (0–500 ms) from “blue”–”yellow”/”dim”–”bright” or vice versa. Data were analysed by paired t test; *** p<0.001, ** p<0.01. (C: left) Responses of cells from A to selective modulation of LWS or UVS opsin excitation, indicating “blue”-ON/”yellow-OFF”, “yellow-ON”/”blue-OFF” or non-opponent responses (conventions as in A). (C: right) Normalised mean (±SEM) change in firing for SCN cell populations evoked by LWS and UVS opsin isolating stimuli. Note, normalisation and scaling for data in A and C is identical. The data used to make this figure can be found in S2 Data.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4401556&req=5

pbio.1002127.g002: Colour opponent responses in suprachiasmatic neurons.(A: left) Example responses of 5 SCN neurons to stimuli modulating UVS and LWS opsin excitation in antiphase (“colour”) or in unison (“brightness”; both 70% Michelson contrast). Individual cells were preferentially excited by blue–yellow transitions (“blue ON”; pink traces), yellow-blue transitions (“yellow ON”; green traces) or dim-bright transitions (“achromatic”; black traces). Shaded areas represent blue/yellow or dim/bright stimulus phase; y-axis scale bars reflects peak firing rate in spikes/s; x-axis scale bars indicate temporal profile of UVS/LWS opsin excitation. (A: right) Normalised mean (±SEM) change in firing for cells classified as “blue-ON”, “yellow-ON” or achromatic (n = 13, 4 and 26 respectively). Conventions as above. (B) Mean (±SEM) firing rates of SCN cell populations tested with colour and brightness stimuli immediately following transitions (0–500 ms) from “blue”–”yellow”/”dim”–”bright” or vice versa. Data were analysed by paired t test; *** p<0.001, ** p<0.01. (C: left) Responses of cells from A to selective modulation of LWS or UVS opsin excitation, indicating “blue”-ON/”yellow-OFF”, “yellow-ON”/”blue-OFF” or non-opponent responses (conventions as in A). (C: right) Normalised mean (±SEM) change in firing for SCN cell populations evoked by LWS and UVS opsin isolating stimuli. Note, normalisation and scaling for data in A and C is identical. The data used to make this figure can be found in S2 Data.
Mentions: To achieve the largest possible change in colour, we started by selectively modulating UVS and LWS cone opsin excitation in antiphase (“colour”; S1B Fig). We then compared responses to this stimulus with those elicited by one in which the change in UVS and LWS opsin activation occurred in unison (“brightness”; S1B Fig). Any spectrally opponent cells should be more responsive to the “colour” as opposed to “brightness” condition. We found that 17/43 SCN units (from 15 mice) that responded to these stimuli showed a significant preference for the pair in which UVS and LWS activation was modulated in antiphase (Fig 2A and 2B; paired t test, p<0.05, n = 17). As there were an additional 26 visually responsive units that did not respond to either of these analytical stimuli (paired t tests, p>0.05), these data indicate that at least one quarter of light-responsive SCN neurones show chromatic opponency.

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