The spectral, angular and polarization sensitivities of photoreceptors in the compound eye of the monarch butterfly (Danaus plexippus) are examined using electrophysiological methods. Intracellular recordings reveal a spectrally homogenous population of UV receptors with optical axes directed upwards and >or=10 degrees to the contralateral side. Based on optical considerations and on the opsin expression pattern (Sauman et al. 2005), we conclude that these UV receptors belong to the anatomically specialized dorsal rim area (DRA) of the eye. Photoreceptors in the main retina with optical axes <10 degrees contralateral or ipsilateral have maximal sensitivities in the UV (lambda(max)<or=340 nm), the blue (lambda(max)=435 nm) or in the long-wave range (green, lambda(max)=540 nm). The polarization sensitivity (PS) of the UV receptors in the DRA is much higher (PS=9.4) than in the UV cells (PS=2.9) or green cells (PS=2.8) of the main retina. The physiological properties of the photoreceptors in the DRA and in the main retina fit closely with the anatomy and the opsin expression patterns described in these eye regions. The data are discussed in the light of present knowledge about polarized skylight navigation in Lepidopterans.