Mammalian circadian rhythms are orchestrated by the suprachiasmatic nuclei (SCN) of the hypothalamus. The SCN are composed of circadian clock neurons, but the mechanisms by which these populations of neuronal oscillators encode rhythmic behavior are incompletely understood. We have used ex vivo real-time gene expression imaging of the neural correlates of circadian behavior, combined with genetic disruption of vasoactive intestinal polypeptide, a key SCN signaling molecule, to examine the neural basis of circadian organization in the SCN. We show that the coherence and timing of clock neuron rhythms are correlated with the coherence and timing of behavioral rhythms within individual mice and that the degree of disruption of SCN neuronal organization correlates with the degree of behavioral disruption within individuals. Our results suggest that the SCN encode circadian phase as a temporal population vector of its constituent neurons; such that as the neuronal population becomes desynchronized, phase information becomes ambiguous.