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Using light to tell the time of day: sensory coding in the mammalian circadian visual network.

Brown TM - J. Exp. Biol. (2016)

Bottom Line: In mammals, these changes are exclusively detected in the retina and are relayed by direct and indirect neural pathways to the master circadian clock in the hypothalamic suprachiasmatic nuclei.Recent work reveals a surprising level of complexity in this sensory control of the circadian system, including the participation of multiple photoreceptive pathways conveying distinct aspects of visual and/or time-of-day information.In this Review, I summarise these important recent advances, present hypotheses as to the functions and neural origins of these sensory signals, highlight key challenges for future research and discuss the implications of our current knowledge for animals and humans in the modern world.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, UK timothy.brown@manchester.ac.uk.

No MeSH data available.


Related in: MedlinePlus

Colour and brightness as indicators of time of day. (A) Spectral irradiance of ‘average’ daylight measured when the sun is 6 deg above or below the horizon. Note that, in addition to the pronounced difference in the amount of light, there is also a substantial change in spectral composition, with reduced middle-wavelength (‘green-yellow’) light at negative solar angles. (B) Sensitivity profiles of the four visual opsin proteins responsible for photoreception in mice, illustrating the distinction between colour and brightness: monochromatic light at 365 and 582 nm produces identical activation of mouse M-opsin but differs in apparent ‘colour’ because the longer wavelength light provides much weaker activation of S-opsin. Importantly, 582 nm light also appears substantially ‘dimmer’ for both rods (rhodopsin) and melanopsin. (C) Top, approximate corneal irradiance, weighted according to mouse rod and melanopsin sensitivity, between midnight and midday on a typical equinox day (clear sky, no moon). Bars to the right indicate effective sensitivity ranges for rod-, melanopsin- and cone-based responses (see Lucas et al., 2012). Bottom, apparent colour of daylight for the mouse visual system (ratio of effective irradiance weighted according to M- versus S-cone opsin sensitivity), demonstrating a progressive shift towards ‘yellow’ with increasing solar elevation. Nocturnal irradiance levels (solar angles <7 deg below horizon) were estimated based on commonly reported values for clear night skies. Apparent colour under these conditions is not relevant because irradiance falls below the threshold for cone-based vision (>10 log photons cm−2 s−1). (D) Apparent rod and melanopsin irradiance (left) and colour (right) as a function of solar angle for six real dawn-to-dusk transitions. In both cases, traces are colour coded, with lighter lines corresponding to days with higher overall irradiance (i.e. less cloud cover). Note that although cloud can reduce irradiance substantially (∼10-fold here), colour remains relatively unaffected. Data in A–D are derived from the dataset presented in Walmsley et al. (2015) (collected in Manchester, UK; 31 Aug–14 Oct 2005).
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JEB132167F2: Colour and brightness as indicators of time of day. (A) Spectral irradiance of ‘average’ daylight measured when the sun is 6 deg above or below the horizon. Note that, in addition to the pronounced difference in the amount of light, there is also a substantial change in spectral composition, with reduced middle-wavelength (‘green-yellow’) light at negative solar angles. (B) Sensitivity profiles of the four visual opsin proteins responsible for photoreception in mice, illustrating the distinction between colour and brightness: monochromatic light at 365 and 582 nm produces identical activation of mouse M-opsin but differs in apparent ‘colour’ because the longer wavelength light provides much weaker activation of S-opsin. Importantly, 582 nm light also appears substantially ‘dimmer’ for both rods (rhodopsin) and melanopsin. (C) Top, approximate corneal irradiance, weighted according to mouse rod and melanopsin sensitivity, between midnight and midday on a typical equinox day (clear sky, no moon). Bars to the right indicate effective sensitivity ranges for rod-, melanopsin- and cone-based responses (see Lucas et al., 2012). Bottom, apparent colour of daylight for the mouse visual system (ratio of effective irradiance weighted according to M- versus S-cone opsin sensitivity), demonstrating a progressive shift towards ‘yellow’ with increasing solar elevation. Nocturnal irradiance levels (solar angles <7 deg below horizon) were estimated based on commonly reported values for clear night skies. Apparent colour under these conditions is not relevant because irradiance falls below the threshold for cone-based vision (>10 log photons cm−2 s−1). (D) Apparent rod and melanopsin irradiance (left) and colour (right) as a function of solar angle for six real dawn-to-dusk transitions. In both cases, traces are colour coded, with lighter lines corresponding to days with higher overall irradiance (i.e. less cloud cover). Note that although cloud can reduce irradiance substantially (∼10-fold here), colour remains relatively unaffected. Data in A–D are derived from the dataset presented in Walmsley et al. (2015) (collected in Manchester, UK; 31 Aug–14 Oct 2005).

Mentions: Thus, the photoentrainment pathway is optimised to signal the changes in illumination associated with twilight, whereas temporal gating modulates the amplitude and direction of the responses (Nelson and Takahashi, 1991). Together, these mechanisms ensure that circadian resetting only occurs around day–night transitions. Although this conceptual model appears sufficient to explain how animals synchronise their clocks to the solar day, the amount of light is not the only source of photic information that reliably changes around twilight. Indeed, the spectral composition (colour) of light reaching the earth also exhibits predictable changes (Fig. 2A), as a result of variations in atmospheric filtering (Hulburt, 1953). The idea that animals might use this variation in colour as a circadian time cue was suggested many years ago (Roenneberg and Foster, 1997) but, owing to the technical difficulties inherent in distinguishing responses to the colour versus brightness of light, it was only recently tested in mammals (Walmsley et al., 2015; see below).Fig. 2.


Using light to tell the time of day: sensory coding in the mammalian circadian visual network.

Brown TM - J. Exp. Biol. (2016)

Colour and brightness as indicators of time of day. (A) Spectral irradiance of ‘average’ daylight measured when the sun is 6 deg above or below the horizon. Note that, in addition to the pronounced difference in the amount of light, there is also a substantial change in spectral composition, with reduced middle-wavelength (‘green-yellow’) light at negative solar angles. (B) Sensitivity profiles of the four visual opsin proteins responsible for photoreception in mice, illustrating the distinction between colour and brightness: monochromatic light at 365 and 582 nm produces identical activation of mouse M-opsin but differs in apparent ‘colour’ because the longer wavelength light provides much weaker activation of S-opsin. Importantly, 582 nm light also appears substantially ‘dimmer’ for both rods (rhodopsin) and melanopsin. (C) Top, approximate corneal irradiance, weighted according to mouse rod and melanopsin sensitivity, between midnight and midday on a typical equinox day (clear sky, no moon). Bars to the right indicate effective sensitivity ranges for rod-, melanopsin- and cone-based responses (see Lucas et al., 2012). Bottom, apparent colour of daylight for the mouse visual system (ratio of effective irradiance weighted according to M- versus S-cone opsin sensitivity), demonstrating a progressive shift towards ‘yellow’ with increasing solar elevation. Nocturnal irradiance levels (solar angles <7 deg below horizon) were estimated based on commonly reported values for clear night skies. Apparent colour under these conditions is not relevant because irradiance falls below the threshold for cone-based vision (>10 log photons cm−2 s−1). (D) Apparent rod and melanopsin irradiance (left) and colour (right) as a function of solar angle for six real dawn-to-dusk transitions. In both cases, traces are colour coded, with lighter lines corresponding to days with higher overall irradiance (i.e. less cloud cover). Note that although cloud can reduce irradiance substantially (∼10-fold here), colour remains relatively unaffected. Data in A–D are derived from the dataset presented in Walmsley et al. (2015) (collected in Manchester, UK; 31 Aug–14 Oct 2005).
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JEB132167F2: Colour and brightness as indicators of time of day. (A) Spectral irradiance of ‘average’ daylight measured when the sun is 6 deg above or below the horizon. Note that, in addition to the pronounced difference in the amount of light, there is also a substantial change in spectral composition, with reduced middle-wavelength (‘green-yellow’) light at negative solar angles. (B) Sensitivity profiles of the four visual opsin proteins responsible for photoreception in mice, illustrating the distinction between colour and brightness: monochromatic light at 365 and 582 nm produces identical activation of mouse M-opsin but differs in apparent ‘colour’ because the longer wavelength light provides much weaker activation of S-opsin. Importantly, 582 nm light also appears substantially ‘dimmer’ for both rods (rhodopsin) and melanopsin. (C) Top, approximate corneal irradiance, weighted according to mouse rod and melanopsin sensitivity, between midnight and midday on a typical equinox day (clear sky, no moon). Bars to the right indicate effective sensitivity ranges for rod-, melanopsin- and cone-based responses (see Lucas et al., 2012). Bottom, apparent colour of daylight for the mouse visual system (ratio of effective irradiance weighted according to M- versus S-cone opsin sensitivity), demonstrating a progressive shift towards ‘yellow’ with increasing solar elevation. Nocturnal irradiance levels (solar angles <7 deg below horizon) were estimated based on commonly reported values for clear night skies. Apparent colour under these conditions is not relevant because irradiance falls below the threshold for cone-based vision (>10 log photons cm−2 s−1). (D) Apparent rod and melanopsin irradiance (left) and colour (right) as a function of solar angle for six real dawn-to-dusk transitions. In both cases, traces are colour coded, with lighter lines corresponding to days with higher overall irradiance (i.e. less cloud cover). Note that although cloud can reduce irradiance substantially (∼10-fold here), colour remains relatively unaffected. Data in A–D are derived from the dataset presented in Walmsley et al. (2015) (collected in Manchester, UK; 31 Aug–14 Oct 2005).
Mentions: Thus, the photoentrainment pathway is optimised to signal the changes in illumination associated with twilight, whereas temporal gating modulates the amplitude and direction of the responses (Nelson and Takahashi, 1991). Together, these mechanisms ensure that circadian resetting only occurs around day–night transitions. Although this conceptual model appears sufficient to explain how animals synchronise their clocks to the solar day, the amount of light is not the only source of photic information that reliably changes around twilight. Indeed, the spectral composition (colour) of light reaching the earth also exhibits predictable changes (Fig. 2A), as a result of variations in atmospheric filtering (Hulburt, 1953). The idea that animals might use this variation in colour as a circadian time cue was suggested many years ago (Roenneberg and Foster, 1997) but, owing to the technical difficulties inherent in distinguishing responses to the colour versus brightness of light, it was only recently tested in mammals (Walmsley et al., 2015; see below).Fig. 2.

Bottom Line: In mammals, these changes are exclusively detected in the retina and are relayed by direct and indirect neural pathways to the master circadian clock in the hypothalamic suprachiasmatic nuclei.Recent work reveals a surprising level of complexity in this sensory control of the circadian system, including the participation of multiple photoreceptive pathways conveying distinct aspects of visual and/or time-of-day information.In this Review, I summarise these important recent advances, present hypotheses as to the functions and neural origins of these sensory signals, highlight key challenges for future research and discuss the implications of our current knowledge for animals and humans in the modern world.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, UK timothy.brown@manchester.ac.uk.

No MeSH data available.


Related in: MedlinePlus