Characterization of orderly spatiotemporal patterns of clock gene activation in mammalian suprachiasmatic nucleus

Apr 15, 2011The European journal of neuroscience

Organized timing and location of daily clock gene activity in the brain’s master timekeeper

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Abstract

Circadian oscillation is characterized by a stable daily cycle of PER2 expression in specific subregions of the suprachiasmatic nucleus (SCN).

Individual cells in the SCN can sustain circadian oscillations but require network interactions for stability.
Cluster analysis of bioluminescence in brain slices shows orderly serial activation of specific SCN subregions.
A silent interval follows the activation of PER2 expression, indicating a structured oscillation pattern.
Symmetry in PER2 expression patterns is observed between the left and right sides of the SCN.
The precise timing of PER2 expression in neurons is influenced by their location within the SCN.

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Because we can observe oscillation within individual cells and in the tissue as a whole, the suprachiasmatic nucleus (SCN) presents a unique system in the mammalian brain for the analysis of individual cells and the networks of which they are a part. While dispersed cells of the SCN sustain circadian oscillations in isolation, they are unstable oscillators that require network interactions for robust cycling. Using cluster analysis to assess bioluminescence in acute brain slices from PERIOD2::Luciferase (PER2::LUC) knockin mice, and immunochemistry of SCN from animals harvested at various circadian times, we assessed the spatiotemporal activation patterns of PER2 to explore the emergence of a coherent oscillation at the tissue level. The results indicate that circadian oscillation is characterized by a stable daily cycle of PER2 expression involving orderly serial activation of specific SCN subregions, followed by a silent interval, with substantial symmetry between the left and right side of the SCN. The biological significance of the clusters identified in living slices was confirmed by co-expression of LUC and PER2 in fixed, immunochemically stained brain sections, with the spatiotemporal pattern of LUC expression resembling that revealed in the cluster analysis of bioluminescent slices. We conclude that the precise timing of PER2 expression within individual neurons is dependent on their location within the nucleus, and that small groups of neurons within the SCN give rise to distinctive and identifiable subregions. We propose that serial activation of these subregions is the basis of robustness and resilience of the daily rhythm of the SCN.

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Characterization of orderly spatiotemporal patterns of clock gene activation in mammalian suprachiasmatic nucleus

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