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Circadian Responses to Fragmented Light: Research Synopsis in Humans

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Circadian Responses to Fragmented Light: Research Synopsis in Humans YALE JOURNAL OF BIOLOGY AND MEDICINE 92 (2019), pp.337-348. Mini-Review Circadian Responses to Fragmented Light: Research Synopsis in Humans Fabian Fernandez* Departments of Psychology, Neurology, the BIO5 Institute, and Evelyn F. McKnight Brain Institute, University of Arizona, Tucson, AZ Light is the chief signal used by the human circadian pacemaker to maintain precise biological timekeeping. Though it has been historically assumed that light resets the pacemaker’s rhythm in a dose-dependent fashion, a number of studies report enhanced circadian photosensitivity to the initial moments of light exposure, such that there are quickly diminishing returns on phase-shifting the longer the light is shown. In the current review, we summarize findings from a family of experiments conducted over two decades in the research wing of the Brigham and Women’s Hospital that examined the human pacemaker’s responses to standardized changes in light patterns generated from an overhead fluorescent ballast. Across several hundred days of laboratory recording, the research group observed phase-shifts in the body temperature and melatonin rhythms that scaled with illuminance. However, as suspected, phase resetting was optimized when exposure occurred as a series of minute-long episodes separated by periods of intervening darkness. These observations set the stage for a more recent program of study at Stanford University that evaluated whether the human pacemaker was capable of integrating fragmented bursts of light in much the same way it perceived steady luminance. The results here suggest that ultra-short durations of light—lasting just 1-2 seconds in total—can elicit pacemaker responses rivaling those created by continuous hour-long stimulation if those few seconds of light are evenly distributed across the hour as discreet 2-millisecond pulses. We conclude our review with a brief discussion of these findings and their potential application in future phototherapy techniques. INTRODUCTION ties critical for reproductive success and survival [2]. In mammals, the light and dark signals that serve to syn- The circadian pacemaker is a biologically conserved chronize the central pacemaker are processed through the timekeeping system that evolved to anticipate daily re- retinohypothalamic tract [3-5]. Photoreceptors in the ret- curring changes in the environment produced by the solar ina provide the sole input into this pathway, which sends light-dark cycle [1]. This anticipation grants organisms, information about light transitions in the environment from unicellular prokaryotic cyanobacteria to multicellu- (i.e., dawn and dusk) and photoperiod length directly to lar eukaryotes, the ability to optimize timing of activi- the central pacemaker neurons seated within the supra- *To whom all correspondence should be addressed: Fabian Fernandez, PhD, Department of Psychology, 1501 N. Campbell Avenue Life Sciences North, Room 349, Tucson, Arizona, 85724; Email: [email protected]. †Abbreviations: SCN, suprachiasmatic nucleus; CBTmin, core body temperature minimum; DLMO, dim-light melatonin onset; h, hour; LED, light-emitting diode; PRC, phase response curve. Keywords: Circadian, Phase shifting, Phototherapy, Light treatment, Light fractionation, Millisecond flashes, Intermittent, Pulse Author Contributions: FF planned the outline of the review, wrote the manuscript, and designed the figures. Copyright © 2019 337 338 Fernandez: Light fractionation chiasmatic nucleus (SCN†) [6-8]. On a daily basis, light the offsets/onsets of the light schedule are also routinely resets the SCN’s imprecise circadian period to a period observed (Figure 1b-c). The picture that emerges with the closely aligned with the 24-h rotation of the Earth, there- PRC is a simple one: with the addition of photoreceptor by entraining the circadian rhythms of the rest of the body input, the central pacemaker has become an exquisitely to the light/dark schedule of the outside world [9]. The sensitive sunrise and sunset detector. To withstand natu- SCN uses both diffusible chemical signals and “hard- ral selection, nearly every surface dwelling animal on the wired” (multisynaptic) neural circuitry to disseminate planet was obliged to use the same exact data stream of circadian cues to the periphery [10-12]. These cues orga- twilight information to measure lapses in time, whether nize peripheral oscillators operating in the body’s organs their species started with the necessary nervous system so that major physiological processes—such as digestion hardware (or clock molecules) to do so or not. Because of and nutrient absorption—are coordinated with one an- this, circadian pacemakers are considered an exemplar of other and optimized for times-of-day when, for example, convergent evolution [24]. food is most readily available [13,14]. ATTEMPTS TO EXPLAIN CIRCADIAN THE PHASE RESPONSE CURVE TO LIGHT RESPONSES TO LIGHT THROUGH RECIPROCITY: ANIMAL STUDIES The pacemaker’s timekeeping adjustments to nat- ural light are often modeled by a sinusoidal-like phase Despite the progress that has been made in elucidat- response curve (PRC) that has been documented in many ing the nature of the molecular machinery responsible for species to date through the use of electric light sources circadian oscillations in cells [25-27], relatively little is (Figure 1a) [15]. Electric light administered in the first known about how the pacemaker, as a “systems unit,” half of the evening invariably triggers a phase delay in samples from the naturally occurring light and darkness one’s subjective schedule of physiology and behavior, it receives, and then factors in differences in irradiance, while later administration in the second half causes a spectral quality, and probability of exposure to deduce phase advance (by convention, the magnitude of the de- geophysical time. One strategy that many investigators lay and advance shifts mobilized by light are plotted with have used to begin to deconstruct this logic is to assess negative and positive numbers, respectively; Figure 1a) what parameters guide the pacemaker’s short-term reac- [16,17]. The shape of the PRC, which can be adapted to tion to nighttime photic stimulation with incandescent or different seasonal photoperiods, likely reflects an entrain- cool fluorescent lamps [28]. Construction of electric light ment logic designed to maintain the temporal niche of an PRCs across a variety of animal models has continued animal [18]. If light in the early evening is perceived as to reaffirm that the single most important variable driv- an extension of the sunset—and that seen in the latter half ing the magnitude and direction of a phase shift is the the leading edge of a sunrise—then such phase regulation precise timing of light administration [15,29]. However, would maximize the contact that diurnal animals have within the same timeframe of the subjective night, other with the sun and minimize the exposure of nocturnal an- photic variables have also emerged that further influence imals. The amplitude characteristics of the PRC, though phase-shifting. These include the spectral weighting of a different in its particulars from one species to the next, light pulse and its brightness or length [30,31], along with bear out this suggestion. the light level or duration of lighting under which a per- The most sensitive parts of the delay and advance son or animal is housed (i.e., dim light histories in either zones can be found several hours after dusk (Figure 1b) case amplify phase-shifting responses to sub-saturating and several hours before dawn (Figure 1c), respectively. light stimuli) [32,33]. Based on knowledge regarding the If electric light presented in these areas affects the circa- biophysical properties of ocular photoreceptors, recent dian system the same as sunlight, then this would alter studies have expanded the parameter space in sophisticat- the pacemaker’s interpretation of the solar cycle, forcing ed ways by showing for instance that different sequences it to manufacture large 2-4-h phase jumps in order to re- of monochromatic light designed to activate—and then align the timing of its internally created day and night to re-sensitize—pacemaker targeting photoreceptors can the newly perceived twilight zones. This is, in fact, what augment phase resetting by maximizing information flow happens after light stimulation in commonly used animal to the pacemaker [34,35]. models such as Drosophila, rodents, as well as humans Recent observations notwithstanding, the historical [16,19-23]. When electric light exposure occurs with- dogma that has organized much of the study on the pace- in the less sensitive parts of the PRC in the 1-2 h of the maker’s relationship with light and darkness is summa- night bookending dusk (lights-off) or dawn (lights-on), rized by the reciprocity hypothesis. It postulates that any smaller phase shifts commensurate in magnitude with the shift made in response to light at a fixed point in the sub- difference in timing between the photic stimulation and jective night results solely from the number of photons Fernandez: Light fractionation 339 Figure 1. A canonical phase response curve to light. (a) Phase-shifts of physiological/behavioral rhythms that result from electric light exposure at night are typically charted with the magnitude of the shifts shown on the y-axis against the timing of light administration on the x-axis. Light’s ability to trigger a circadian response is gated through- out the night, with particular pockets of sensitivity occurring several hours after dusk (b) or several hours before dawn (c). The pattern of these responses suggests that the pacemaker’s photic sensitivity is scaled so that light exposure produces shifts that will always align the pacemaker’s daily rhythm to the transitions of the light-dark cycle under which a person or animal is kept. Please note that not all human PRCs have a “dead zone” of photic insensitivity occurring during the subjective day. Depending on the stimulation protocol, some may take highly linear shapes, with a constant negative slope traveling between the advance and delay regions [73].
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