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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

Temporal gating and integration in the circadian system. (A–C) Schematic ‘actograms’ showing daily activity (black bars) for nocturnal (A,B) or diurnal (C) mammals under a light:dark (L:D) cycle and following transfer to constant conditions to reveal the biological clock's intrinsic period; here either shorter (A; 23.5 h) or longer (B,C; 24.5 h) than 24 h. In each case, light pulses (red circles) presented around the animal's subjective evening (‘dusk’) delay the onset of activity on subsequent days, whereas light pulses presented during the subjective morning (‘dawn’) advance activity onset. (D,E) Phase-response curves (PRCs) quantifying the change in activity onset as a function of the circadian time at which light is detected for bright and dim light (circadian time 12 designated as the onset of subjective night). Note that PRCs for individuals with fast clocks are characterised by large delay and small advance portions (D) and vice versa for individuals with slow internal clocks (E). As such, organisms with fast clocks primarily use dusk light for entrainment (because these require a daily phase delay to bring their endogenous period up to that of the 24 h solar day), whereas organisms with slow clocks primarily use dawn light (because these require a daily advance to maintain 24 h rhythms). In all plots, periods of light are indicated by white backgrounds and periods of darkness are indicated by grey backgrounds.
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JEB132167F1: Temporal gating and integration in the circadian system. (A–C) Schematic ‘actograms’ showing daily activity (black bars) for nocturnal (A,B) or diurnal (C) mammals under a light:dark (L:D) cycle and following transfer to constant conditions to reveal the biological clock's intrinsic period; here either shorter (A; 23.5 h) or longer (B,C; 24.5 h) than 24 h. In each case, light pulses (red circles) presented around the animal's subjective evening (‘dusk’) delay the onset of activity on subsequent days, whereas light pulses presented during the subjective morning (‘dawn’) advance activity onset. (D,E) Phase-response curves (PRCs) quantifying the change in activity onset as a function of the circadian time at which light is detected for bright and dim light (circadian time 12 designated as the onset of subjective night). Note that PRCs for individuals with fast clocks are characterised by large delay and small advance portions (D) and vice versa for individuals with slow internal clocks (E). As such, organisms with fast clocks primarily use dusk light for entrainment (because these require a daily phase delay to bring their endogenous period up to that of the 24 h solar day), whereas organisms with slow clocks primarily use dawn light (because these require a daily advance to maintain 24 h rhythms). In all plots, periods of light are indicated by white backgrounds and periods of darkness are indicated by grey backgrounds.

Mentions: Early experiments in the field investigated the effects of light on circadian patterns of voluntary activity in various nocturnal rodent species (Daan and Pittendrigh, 1976; DeCoursey, 1960, 1964). These experiments established a key principle underlying circadian photoentrainment: responses to light vary predictably depending on time of day (temporal gating; see Glossary). Hence, light exposure in the early night shifts activity to later time points (phase delays), light in the late night shifts activity to earlier time points (phase advances) and light has no effect during the middle of the day (Fig. 1). This is also true in diurnal mammals, including humans (Hoban and Sulzman, 1985; Kas and Edgar, 2000; Khalsa et al., 2003; Mahoney et al., 2001). Indeed, this mechanism is characteristic of the majority of organisms, although with certain interspecific (Pittendrigh, 1988) and intraspecific (Daan and Pittendrigh, 1976; DeCoursey, 1960) differences: the relative size of phase advances and delays depends on the endogenous circadian period – fast clocks (periods <24 h) are associated with larger delays, whereas slow clocks (periods >24 h) are associated with larger advances. This arrangement ensures a stable period and phase of the internal clock relative to the strictly 24 h solar cycle (Fig. 1).Fig. 1.


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

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

Temporal gating and integration in the circadian system. (A–C) Schematic ‘actograms’ showing daily activity (black bars) for nocturnal (A,B) or diurnal (C) mammals under a light:dark (L:D) cycle and following transfer to constant conditions to reveal the biological clock's intrinsic period; here either shorter (A; 23.5 h) or longer (B,C; 24.5 h) than 24 h. In each case, light pulses (red circles) presented around the animal's subjective evening (‘dusk’) delay the onset of activity on subsequent days, whereas light pulses presented during the subjective morning (‘dawn’) advance activity onset. (D,E) Phase-response curves (PRCs) quantifying the change in activity onset as a function of the circadian time at which light is detected for bright and dim light (circadian time 12 designated as the onset of subjective night). Note that PRCs for individuals with fast clocks are characterised by large delay and small advance portions (D) and vice versa for individuals with slow internal clocks (E). As such, organisms with fast clocks primarily use dusk light for entrainment (because these require a daily phase delay to bring their endogenous period up to that of the 24 h solar day), whereas organisms with slow clocks primarily use dawn light (because these require a daily advance to maintain 24 h rhythms). In all plots, periods of light are indicated by white backgrounds and periods of darkness are indicated by grey backgrounds.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4920240&req=5

JEB132167F1: Temporal gating and integration in the circadian system. (A–C) Schematic ‘actograms’ showing daily activity (black bars) for nocturnal (A,B) or diurnal (C) mammals under a light:dark (L:D) cycle and following transfer to constant conditions to reveal the biological clock's intrinsic period; here either shorter (A; 23.5 h) or longer (B,C; 24.5 h) than 24 h. In each case, light pulses (red circles) presented around the animal's subjective evening (‘dusk’) delay the onset of activity on subsequent days, whereas light pulses presented during the subjective morning (‘dawn’) advance activity onset. (D,E) Phase-response curves (PRCs) quantifying the change in activity onset as a function of the circadian time at which light is detected for bright and dim light (circadian time 12 designated as the onset of subjective night). Note that PRCs for individuals with fast clocks are characterised by large delay and small advance portions (D) and vice versa for individuals with slow internal clocks (E). As such, organisms with fast clocks primarily use dusk light for entrainment (because these require a daily phase delay to bring their endogenous period up to that of the 24 h solar day), whereas organisms with slow clocks primarily use dawn light (because these require a daily advance to maintain 24 h rhythms). In all plots, periods of light are indicated by white backgrounds and periods of darkness are indicated by grey backgrounds.
Mentions: Early experiments in the field investigated the effects of light on circadian patterns of voluntary activity in various nocturnal rodent species (Daan and Pittendrigh, 1976; DeCoursey, 1960, 1964). These experiments established a key principle underlying circadian photoentrainment: responses to light vary predictably depending on time of day (temporal gating; see Glossary). Hence, light exposure in the early night shifts activity to later time points (phase delays), light in the late night shifts activity to earlier time points (phase advances) and light has no effect during the middle of the day (Fig. 1). This is also true in diurnal mammals, including humans (Hoban and Sulzman, 1985; Kas and Edgar, 2000; Khalsa et al., 2003; Mahoney et al., 2001). Indeed, this mechanism is characteristic of the majority of organisms, although with certain interspecific (Pittendrigh, 1988) and intraspecific (Daan and Pittendrigh, 1976; DeCoursey, 1960) differences: the relative size of phase advances and delays depends on the endogenous circadian period – fast clocks (periods <24 h) are associated with larger delays, whereas slow clocks (periods >24 h) are associated with larger advances. This arrangement ensures a stable period and phase of the internal clock relative to the strictly 24 h solar cycle (Fig. 1).Fig. 1.

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