Constant Light Desynchronizes Olfactory versus Object and Visuospatial Recognition Memory Performance

Mar 8, 2017The Journal of neuroscience : the official journal of the Society for Neuroscience

Constant Light Disrupts Smell Memory Differently Than Object and Space Memory

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Abstract

C57BL/6J mice show better recognition performance at midday compared to midnight under standard light/dark cycles.

Recognition performance in object, visuospatial, and olfactory tasks is consistently higher at midday than at midnight under normal lighting conditions.
Under constant light conditions, recognition performance becomes desynchronized, with object and visuospatial tasks peaking at subjective midday and olfactory tasks at subjective midnight.
Changes in recognition performance correspond with altered expression of key clock genes in the suprachiasmatic nuclei (SCN), hippocampus, and olfactory bulb.
While gene expression in the SCN is less rhythmic under constant light, the hippocampus maintains rhythmic expression relating to object and visuospatial performance.
Inversion of olfactory performance is linked to reversed gene expression in the olfactory bulb.
Despite desynchrony in certain brain regions, core body temperature and exploratory activity rhythms continue under constant light.

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optimize physiology and behavior to the varying demands of the 24 h day. The master circadian clock is located in the suprachiasmatic nuclei (SCN) of the hypothalamus and it regulates circadian oscillators in tissues throughout the body to prevent internal desynchrony. Here, we demonstrate for the first time that, under standard 12 h:12 h light/dark (LD) cycles, object, visuospatial, and olfactory recognition performance in C57BL/6J mice is consistently better at midday relative to midnight. However, under repeated exposure to constant light (LL), recognition performance becomes desynchronized, with object and visuospatial performance better at subjective midday and olfactory performance better at subjective midnight. This desynchrony in behavioral performance is mirrored by changes in expression of the canonical clock genesand(and), as well as the immediate-early genein the SCN, dorsal hippocampus, and olfactory bulb. UnderLL, rhythmicandexpression is attenuated in the SCN. In contrast, hippocampal gene expression remains rhythmic, mirroring object and visuospatial performance. Strikingly,andexpression in the olfactory bulb is reversed, mirroring the inverted olfactory performance. Temporal desynchrony among these regions does not result in arrhythmicity because core body temperature and exploratory activity rhythms persist underLL. Our data provide the first demonstration that abnormal lighting conditions can give rise to temporal desynchrony between autonomous circadian oscillators in different regions, with different consequences for performance across different sensory domains. Such a dispersed network of dissociable circadian oscillators may provide greater flexibility when faced with conflicting environmental signals.A master circadian clock in the suprachiasmatic nuclei (SCN) of the hypothalamus regulates physiology and behavior across the 24 h day by synchronizing peripheral clocks throughout the brain and body. Without the SCN, these peripheral clocks rapidly become desynchronized. Here, we provide a unique demonstration that, under lighting conditions in which the central clock in the SCN is dampened, peripheral oscillators in the hippocampus and olfactory bulb become desynchronized, along with the behavioral processes mediated by these clocks. Multiple clocks that adopt different phase relationships may enable processes occurring in different brain regions to be optimized to specific phases of the 24 h day. Moreover, such a dispersed network of dissociable circadian clocks may provide greater flexibility when faced with conflicting environmental signals (e.g., seasonal changes in photoperiod). r Period1Period2Per1Per2Fos r Per1Fos Per1Fos r SIGNIFICANCE STATEMENT

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Object Recognition Performance

Mice tested under LD at ZT 6 for object recognition.

Olfactory Recognition Performance Shift

Mice tested under LL at CT 18 for olfactory recognition.

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Constant Light Desynchronizes Olfactory versus Object and Visuospatial Recognition Memory Performance

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