The anterior optic tubercle is a small neuropil in the insect brain and a major target of visual interneurons from the optic lobe. The functional role of the tubercle is poorly understood, but recent evidence from locusts points to a possible involvement in polarization vision. The present study examines the organization of the anterior optic tubercle in the locust Schistocerca gregaria and its connections with other brain areas. The tubercle of the locust consists of an upper and a lower subunit. Both units are connected in parallel with the medulla and lobula of the optic lobe, with the contralateral tubercle, and with the lateral accessory lobe in the median protocerebrum. Wide-field transmedullary neurons provide input from the medulla. Neurons with processes in the dorsal rim of the medulla, a relay station in the polarization vision pathway, project exclusively to the lower unit of the tubercle. Visual input from the lobula to the upper and lower unit originates from topographically distinct strata. The most prominent output target of the tubercle is the lateral accessory lobe in the median protocerebrum. Neurons from the upper unit project widely in the lateral accessory lobe, whereas neurons from the lower unit have focused projections confined to the median olive and to the lateral triangle. The two subunits of the anterior optic tubercle are, therefore, processing stages in two parallel visual pathways from the optic lobe to the median protocerebrum. Pathways via the lower unit of the tubercle appear to be involved in polarization vision.

Histamine serves a neurotransmitter role in arthropod photoreceptor neurons, but is also present in a small number of interneurons throughout the nervous system. In search of a suitable model system for the analysis of histaminergic neurotransmission in insects, we mapped the distribution of histamine in the brain of the desert locust Schistocerca gregaria by immunocytochemistry. In the optic lobe, apparently all photoreceptor cells of the compound eye with projections to the lamina and medulla showed intense immunostaining. Photoreceptors of the dorsal rim area of the eye had particularly large fiber diameters and gave rise to uniform varicose immunostaining throughout dorsal rim areas of the lamina and medulla. In the locust midbrain 21 bilateral pairs of histamine-immunoreactive interneurons were found, and 13 of these were reconstructed in detail. While most neuropil areas contained a dense meshwork of immunoreactive processes, immunostaining in the antennal lobe and in the calyces of the mushroom body was sparse and no staining occurred in the pedunculus and lobes of the mushroom body, in the protocerebral bridge, and in the lower division of the central body. A prominent group of four immunostained neurons had large cell bodies near the median ocellar nerve root and descending axonal fibers. These neurons are probably identical to previously identified primary commissure pioneer neurons of the locust brain. The apparent lack in the desert locust of certain histamine-immunoreactive neurons which were reported in the migratory locust may be responsible for differences in the physiological role of histamine between both species.

The polarization pattern of the blue sky serves as an important reference for spatial orientation in insects. To understand the neural mechanisms involved in sky compass orientation we have analyzed the polarization vision system in the locust Schistocerca gregaria. As in other insects, photoreceptors adapted for the detection of sky polarization are concentrated in a dorsal rim area (DRA) of the compound eye. Stationary flying locusts show polarotactic yaw-torque responses when illuminated through a rotating polarizer from above. This response is abolished after painting the DRAs. Central stages of the polarization vision system, revealed through tracing studies, include dorsal areas in the lamina and medulla, the anterior lobe of the lobula, the anterior optic tubercle, the lateral accessory lobe and the central complex. Physiological analysis of polarization-sensitive (POL) neurons has focussed on the optic tubercle and on the central complex. Each POL neuron was maximally excited at a certain e-vector (phimax) and was maximally inhibited at an e-vector perpendicular to phimax. The neurons had large visual fields, and many neurons received input from both eyes. The neuronal organization of the central complex suggests a role as a spatial compass within the locust brain.