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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

Sensory properties of mouse SCN neurons. (A) Characteristic response profiles of different classes of light-responsive SCN neurons in the mouse (normalised to maximal firing), revealed using stimuli that activate all classes of retinal photoreceptors (blue lines) versus those that strongly activate rods and cones but not melanopsin (red lines; means±s.e.m.; cells recorded as part of Brown et al., 2011). Note that although most cells receive both rod/cone and melanopsin input (‘sustained’), less commonly encountered cells show very little melanopsin response (‘transient’) or show sluggish increases or decreases in firing that are primarily driven by melanopsin (bottom panel). (B) The relative size of melanopsin-driven responses in ‘sustained’ SCN cells as a function of circadian time (mean±s.e.m.; derived from data in Brown et al., 2011) is a significantly larger change than observed in mRGCs themselves (range indicated by dashed lines; see Weng et al., 2009). (C) The sensitivity range of light-evoked SCN firing (for stimuli providing equal activation of all photoreceptor classes; Walmsley and Brown, 2015) is substantially narrower than that reported for mRGCs (represented by the blue bar; Dacey et al., 2005; Wong et al., 2007; Weng et al., 2013). (D) The diversity in cone-driven responses of SCN cells, determined using stimuli that selectively activate individual cone opsin classes (means±s.e.m.; based on data in Walmsley et al., 2015). A subset of SCN cells exhibit chromatic opponency, most commonly ‘blue-ON/yellow-OFF’ (top), whereas other cells show excitatory responses to activation of both cone opsin classes (bottom). For the plots shown in A, B and D, white backgrounds indicate periods of light and grey backgrounds indicate periods of darkness. For A and D, the percentage of cells that fall into each class is indicated in the upper right corner.
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JEB132167F4: Sensory properties of mouse SCN neurons. (A) Characteristic response profiles of different classes of light-responsive SCN neurons in the mouse (normalised to maximal firing), revealed using stimuli that activate all classes of retinal photoreceptors (blue lines) versus those that strongly activate rods and cones but not melanopsin (red lines; means±s.e.m.; cells recorded as part of Brown et al., 2011). Note that although most cells receive both rod/cone and melanopsin input (‘sustained’), less commonly encountered cells show very little melanopsin response (‘transient’) or show sluggish increases or decreases in firing that are primarily driven by melanopsin (bottom panel). (B) The relative size of melanopsin-driven responses in ‘sustained’ SCN cells as a function of circadian time (mean±s.e.m.; derived from data in Brown et al., 2011) is a significantly larger change than observed in mRGCs themselves (range indicated by dashed lines; see Weng et al., 2009). (C) The sensitivity range of light-evoked SCN firing (for stimuli providing equal activation of all photoreceptor classes; Walmsley and Brown, 2015) is substantially narrower than that reported for mRGCs (represented by the blue bar; Dacey et al., 2005; Wong et al., 2007; Weng et al., 2013). (D) The diversity in cone-driven responses of SCN cells, determined using stimuli that selectively activate individual cone opsin classes (means±s.e.m.; based on data in Walmsley et al., 2015). A subset of SCN cells exhibit chromatic opponency, most commonly ‘blue-ON/yellow-OFF’ (top), whereas other cells show excitatory responses to activation of both cone opsin classes (bottom). For the plots shown in A, B and D, white backgrounds indicate periods of light and grey backgrounds indicate periods of darkness. For A and D, the percentage of cells that fall into each class is indicated in the upper right corner.

Mentions: The basic properties of light-responsive SCN neurons have been assessed in various nocturnal (Brown et al., 2011; Meijer et al., 1986; Mure et al., 2007; Walmsley and Brown, 2015) and diurnal mammals (Groos and Mason, 1980; Jiao et al., 1999; Meijer et al., 1989). These experiments reveal a characteristic feature of the SCN light response: sustained increases or decreases in electrical discharge that are proportional to the intensity of illumination. Although these irradiance-coding properties broadly align with the properties of the mRGCs that provide this input, several features are worth noting (Fig. 4). Firstly, the sensory properties of SCN neurons seem surprisingly diverse relative to those of mRGCs (Fig. 4A). For example, the presence of light-suppressed cells is surprising, given that mRGCs are exclusively light activated and provide excitatory glutamatergic input to the SCN (Gompf et al., 2015). Secondly, there is a pronounced rhythm in the amplitude of light-evoked SCN activity that cannot simply be explained by daily variations in mRGC input (Fig. 4B; Brown et al., 2011; Meijer et al., 1996, 1998; van Oosterhout et al., 2012), presumably reflecting the intrinsic changes in SCN cell excitability indicated above. Finally, light-dependent modulation of SCN activity seems to require substantially (∼1000-fold) higher levels of illumination than that evoking measureable responses from mRGCs (Fig. 4C) (e.g. compare Brown et al., 2011; Weng et al., 2013).Fig. 4.


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

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

Sensory properties of mouse SCN neurons. (A) Characteristic response profiles of different classes of light-responsive SCN neurons in the mouse (normalised to maximal firing), revealed using stimuli that activate all classes of retinal photoreceptors (blue lines) versus those that strongly activate rods and cones but not melanopsin (red lines; means±s.e.m.; cells recorded as part of Brown et al., 2011). Note that although most cells receive both rod/cone and melanopsin input (‘sustained’), less commonly encountered cells show very little melanopsin response (‘transient’) or show sluggish increases or decreases in firing that are primarily driven by melanopsin (bottom panel). (B) The relative size of melanopsin-driven responses in ‘sustained’ SCN cells as a function of circadian time (mean±s.e.m.; derived from data in Brown et al., 2011) is a significantly larger change than observed in mRGCs themselves (range indicated by dashed lines; see Weng et al., 2009). (C) The sensitivity range of light-evoked SCN firing (for stimuli providing equal activation of all photoreceptor classes; Walmsley and Brown, 2015) is substantially narrower than that reported for mRGCs (represented by the blue bar; Dacey et al., 2005; Wong et al., 2007; Weng et al., 2013). (D) The diversity in cone-driven responses of SCN cells, determined using stimuli that selectively activate individual cone opsin classes (means±s.e.m.; based on data in Walmsley et al., 2015). A subset of SCN cells exhibit chromatic opponency, most commonly ‘blue-ON/yellow-OFF’ (top), whereas other cells show excitatory responses to activation of both cone opsin classes (bottom). For the plots shown in A, B and D, white backgrounds indicate periods of light and grey backgrounds indicate periods of darkness. For A and D, the percentage of cells that fall into each class is indicated in the upper right corner.
© Copyright Policy - open-access
Related In: Results  -  Collection

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JEB132167F4: Sensory properties of mouse SCN neurons. (A) Characteristic response profiles of different classes of light-responsive SCN neurons in the mouse (normalised to maximal firing), revealed using stimuli that activate all classes of retinal photoreceptors (blue lines) versus those that strongly activate rods and cones but not melanopsin (red lines; means±s.e.m.; cells recorded as part of Brown et al., 2011). Note that although most cells receive both rod/cone and melanopsin input (‘sustained’), less commonly encountered cells show very little melanopsin response (‘transient’) or show sluggish increases or decreases in firing that are primarily driven by melanopsin (bottom panel). (B) The relative size of melanopsin-driven responses in ‘sustained’ SCN cells as a function of circadian time (mean±s.e.m.; derived from data in Brown et al., 2011) is a significantly larger change than observed in mRGCs themselves (range indicated by dashed lines; see Weng et al., 2009). (C) The sensitivity range of light-evoked SCN firing (for stimuli providing equal activation of all photoreceptor classes; Walmsley and Brown, 2015) is substantially narrower than that reported for mRGCs (represented by the blue bar; Dacey et al., 2005; Wong et al., 2007; Weng et al., 2013). (D) The diversity in cone-driven responses of SCN cells, determined using stimuli that selectively activate individual cone opsin classes (means±s.e.m.; based on data in Walmsley et al., 2015). A subset of SCN cells exhibit chromatic opponency, most commonly ‘blue-ON/yellow-OFF’ (top), whereas other cells show excitatory responses to activation of both cone opsin classes (bottom). For the plots shown in A, B and D, white backgrounds indicate periods of light and grey backgrounds indicate periods of darkness. For A and D, the percentage of cells that fall into each class is indicated in the upper right corner.
Mentions: The basic properties of light-responsive SCN neurons have been assessed in various nocturnal (Brown et al., 2011; Meijer et al., 1986; Mure et al., 2007; Walmsley and Brown, 2015) and diurnal mammals (Groos and Mason, 1980; Jiao et al., 1999; Meijer et al., 1989). These experiments reveal a characteristic feature of the SCN light response: sustained increases or decreases in electrical discharge that are proportional to the intensity of illumination. Although these irradiance-coding properties broadly align with the properties of the mRGCs that provide this input, several features are worth noting (Fig. 4). Firstly, the sensory properties of SCN neurons seem surprisingly diverse relative to those of mRGCs (Fig. 4A). For example, the presence of light-suppressed cells is surprising, given that mRGCs are exclusively light activated and provide excitatory glutamatergic input to the SCN (Gompf et al., 2015). Secondly, there is a pronounced rhythm in the amplitude of light-evoked SCN activity that cannot simply be explained by daily variations in mRGC input (Fig. 4B; Brown et al., 2011; Meijer et al., 1996, 1998; van Oosterhout et al., 2012), presumably reflecting the intrinsic changes in SCN cell excitability indicated above. Finally, light-dependent modulation of SCN activity seems to require substantially (∼1000-fold) higher levels of illumination than that evoking measureable responses from mRGCs (Fig. 4C) (e.g. compare Brown et al., 2011; Weng et al., 2013).Fig. 4.

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