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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

Melanopsin signals influence both colour- and brightness-sensitive cells.(A) Normalised mean (±SEM) response of blue-ON colour-sensitive (n = 13) and achromatic cells (n = 23 tested) to stimuli targeting melanopsin and/or cones. Melanopsin-isolating stimuli presented a 92% Michelson contrast change (~1.4 log units), all other stimuli were 70% Michelson contrast (see S1A Fig for details of “colour” and “brightness” stimuli). The energy condition reflects a spectrally neutral modulation in light intensity, providing 70% Michelson contrast for all retinal opsins. Far right panels reflect the predicted melanopsin contribution to the 70% energy condition (obtained by subtracting the responses to UVS + LWS only −”brightness”). Responses were normalised on a within-cell basis across all three stimulus conditions and are plotted on the same scale to highlight relative response amplitude. X-axis scale bars indicate temporal profile of UVS/LWS opsin and melanopsin excitation. (B) Example responses of yellow-ON colour-sensitive cells (bottom panels) to stimuli targeting melanopsin and/or cones or melanopsin. Melanopsin-isolating contrast had more heterogeneous effects in yellow-ON cells, with 1/4 cells exhibiting a reduction in firing and 2 cells displaying no obvious response (not shown). Conventions as above except that data are presented as raw firing rates. Y-axis scale bars represent peak firing in spikes/s. The data used to make this figure can be found in S3 Data.
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pbio.1002127.g003: Melanopsin signals influence both colour- and brightness-sensitive cells.(A) Normalised mean (±SEM) response of blue-ON colour-sensitive (n = 13) and achromatic cells (n = 23 tested) to stimuli targeting melanopsin and/or cones. Melanopsin-isolating stimuli presented a 92% Michelson contrast change (~1.4 log units), all other stimuli were 70% Michelson contrast (see S1A Fig for details of “colour” and “brightness” stimuli). The energy condition reflects a spectrally neutral modulation in light intensity, providing 70% Michelson contrast for all retinal opsins. Far right panels reflect the predicted melanopsin contribution to the 70% energy condition (obtained by subtracting the responses to UVS + LWS only −”brightness”). Responses were normalised on a within-cell basis across all three stimulus conditions and are plotted on the same scale to highlight relative response amplitude. X-axis scale bars indicate temporal profile of UVS/LWS opsin and melanopsin excitation. (B) Example responses of yellow-ON colour-sensitive cells (bottom panels) to stimuli targeting melanopsin and/or cones or melanopsin. Melanopsin-isolating contrast had more heterogeneous effects in yellow-ON cells, with 1/4 cells exhibiting a reduction in firing and 2 cells displaying no obvious response (not shown). Conventions as above except that data are presented as raw firing rates. Y-axis scale bars represent peak firing in spikes/s. The data used to make this figure can be found in S3 Data.

Mentions: We next asked whether colour opponent cells also received irradiance information from the melanopsin-expressing ipRGCs that dominate retinal input to the SCN [4,6,7]. To this end, we used changes in spectral composition to selectively modulate melanopsin excitation (see Methods; 14/15 mice above tested with these stimuli). When presented with large steps in melanopsin excitation (92% Michelson contrast) generated in this way, “blue”-ON cells showed slow and sustained increases in firing (Fig 3A; peak response = 3.2 ± 0.8 spikes/s above baseline; paired t test, p<0.01, n = 13), as previously described for melanopsin-driven responses [8,27,28]. The behaviour of the rare “yellow” ON cells to this stimulus was variable (Fig 3B; n = 4), while colour-insensitive cells showed the expected excitatory response (Fig 3A; peak response = 1.8 ± 0.2 spikes/s above baseline; paired t test, p<0.01, n = 23). These data therefore reveal that both chromatic and achromatic cells have access to melanopsin-dependent information about irradiance.


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)

Melanopsin signals influence both colour- and brightness-sensitive cells.(A) Normalised mean (±SEM) response of blue-ON colour-sensitive (n = 13) and achromatic cells (n = 23 tested) to stimuli targeting melanopsin and/or cones. Melanopsin-isolating stimuli presented a 92% Michelson contrast change (~1.4 log units), all other stimuli were 70% Michelson contrast (see S1A Fig for details of “colour” and “brightness” stimuli). The energy condition reflects a spectrally neutral modulation in light intensity, providing 70% Michelson contrast for all retinal opsins. Far right panels reflect the predicted melanopsin contribution to the 70% energy condition (obtained by subtracting the responses to UVS + LWS only −”brightness”). Responses were normalised on a within-cell basis across all three stimulus conditions and are plotted on the same scale to highlight relative response amplitude. X-axis scale bars indicate temporal profile of UVS/LWS opsin and melanopsin excitation. (B) Example responses of yellow-ON colour-sensitive cells (bottom panels) to stimuli targeting melanopsin and/or cones or melanopsin. Melanopsin-isolating contrast had more heterogeneous effects in yellow-ON cells, with 1/4 cells exhibiting a reduction in firing and 2 cells displaying no obvious response (not shown). Conventions as above except that data are presented as raw firing rates. Y-axis scale bars represent peak firing in spikes/s. The data used to make this figure can be found in S3 Data.
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Related In: Results  -  Collection

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

pbio.1002127.g003: Melanopsin signals influence both colour- and brightness-sensitive cells.(A) Normalised mean (±SEM) response of blue-ON colour-sensitive (n = 13) and achromatic cells (n = 23 tested) to stimuli targeting melanopsin and/or cones. Melanopsin-isolating stimuli presented a 92% Michelson contrast change (~1.4 log units), all other stimuli were 70% Michelson contrast (see S1A Fig for details of “colour” and “brightness” stimuli). The energy condition reflects a spectrally neutral modulation in light intensity, providing 70% Michelson contrast for all retinal opsins. Far right panels reflect the predicted melanopsin contribution to the 70% energy condition (obtained by subtracting the responses to UVS + LWS only −”brightness”). Responses were normalised on a within-cell basis across all three stimulus conditions and are plotted on the same scale to highlight relative response amplitude. X-axis scale bars indicate temporal profile of UVS/LWS opsin and melanopsin excitation. (B) Example responses of yellow-ON colour-sensitive cells (bottom panels) to stimuli targeting melanopsin and/or cones or melanopsin. Melanopsin-isolating contrast had more heterogeneous effects in yellow-ON cells, with 1/4 cells exhibiting a reduction in firing and 2 cells displaying no obvious response (not shown). Conventions as above except that data are presented as raw firing rates. Y-axis scale bars represent peak firing in spikes/s. The data used to make this figure can be found in S3 Data.
Mentions: We next asked whether colour opponent cells also received irradiance information from the melanopsin-expressing ipRGCs that dominate retinal input to the SCN [4,6,7]. To this end, we used changes in spectral composition to selectively modulate melanopsin excitation (see Methods; 14/15 mice above tested with these stimuli). When presented with large steps in melanopsin excitation (92% Michelson contrast) generated in this way, “blue”-ON cells showed slow and sustained increases in firing (Fig 3A; peak response = 3.2 ± 0.8 spikes/s above baseline; paired t test, p<0.01, n = 13), as previously described for melanopsin-driven responses [8,27,28]. The behaviour of the rare “yellow” ON cells to this stimulus was variable (Fig 3B; n = 4), while colour-insensitive cells showed the expected excitatory response (Fig 3A; peak response = 1.8 ± 0.2 spikes/s above baseline; paired t test, p<0.01, n = 23). These data therefore reveal that both chromatic and achromatic cells have access to melanopsin-dependent information about irradiance.

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