Descending neurons supplying the neck and flight motor of Diptera: organization and neuroanatomical relationships with visual pathways.

In dipterous insects, a volume of behavioral and electrophysiological studies promote the contention that three wide-field motion-sensitive tangential neurons provide a necessary and sufficient input to specific channels that drive the torque motor during flight. The present studies describe the results of neuroanatomical investigations of the relationships between motion-sensitive neuropil in the fly optic lobes and descending neurons that arise from a restricted area of the brain and supply segmental neck and flight motor neuropil. The present observations resolve at least 50 pairs of descending neurons supplying flight motor centers in the thoracic ganglia. The majority of descending neurons receive a distributed output from horizontal motion-sensitive neurons. However, the same descending neurons are also visited by numerous small-field retinotopic neurons from the lobula plate as well as hitherto undescribed small tangential neurons. Neuroanatomical studies, using cobalt, Golgi, and Texas red histology, demonstrate that these smaller inputs onto descending neurons have dendrites that are organized at specific strata in retinotopic neuropil and that these correspond to horizontal and vertical motion sensitivity layers. Conclusions that only a restricted number of wide-field neurons are necessary and sufficient for visually stabilized flight may be premature. Rather, neuroanatomical evidence suggests that descending neurons to the flight motor may each be selectively tuned to specific combinations of wide- and small-field visual cues, so providing a cooperative descending network controlling the rich repertoire of visually evoked flight behavior.