Neuroimaging studies have explored cerebral activation patterns in patients with cluster headache (CH) during attacks and have revealed activation of multiple brain areas known to belong to the general pain-processing network. However, it is still unclear which changes in brain metabolism are inherent to the shift from the 'in bout' to the 'out of bout' period. We measured cerebral glucose metabolism in 11 episodic CH patients during the cluster and again during the remission period with (18)F-fluoro-2-deoxy-D-glucose-positron emission tomography (FDG-PET) and compared these data with 11 healthy controls. 'In bout' compared with 'out of bout' scans were associated with increases of metabolism in the perigenual anterior cingulate cortex (ACC), posterior cingulate cortex, prefrontal cortex, insula, thalamus and temporal cortex. Decreases in metabolism were observed in the cerebellopontine area. Compared with healthy volunteers, hypometabolism in the patient group ('in bout' and 'out of bout') was found in the perigenual ACC, prefrontal and orbitofrontal cortex. Thus, FDG-PET in CH patients revealed 'in bout' activation of brain structures which are involved in descending pain control. Compared with controls, the regional brain metabolism was constitutively decreased in most of these structures, irrespective of the bout. This finding indicates a deficient top-down modulation of antinociceptive circuits in CH patients. We suggest that trigger mechanisms of CH are insufficiently controlled and thus promote the initiation of the bout period and acute attack.