Max-Planck-Institut für biolgische Kybernetik, Tübingen, F.R.G.
Our objective is to analyze certain aspects of the neuronal circuitry underlying insect walking. Special interest is taken in the role of the head ganglia and, more specifically, the central complex (CC), a conspicuous neuropilar region in the protocerebrum of insects.
The behavioral significance of the CC for walking and certain aspects of orientation was deduced from comparative behavioral studies in Drosophila mutant lines with known structural disorders in the CC (Strauss and Heisenberg 1993 J Neurosci 13:1852-61). In the present study we identified 30 lines with gross morphological CC defects out of 230 walking impaired X-linked lines, the outcome of our behavioral screen of 10750 flies (Strauss 1995 J Neurogenet 10). Considering the neuronal and non-neuronal extent of the walking system this unexpectedly large fraction of 13% of all lines emphasizes its importance as a higher center for locomotor control.
Our automated video-based detector system (Strauss 1993 J Neurogenet 8:250) faciliates the quantitative determination of gait, step length, joint angles, and duration of swing phase. CC-defective and other walking impaired lines were compared with respect to stepping frequency and stride length, the main determinants of walking speed. Our findings show that the CC is involved in the adjustment of step lengths (i) to optimize walking speed, (ii) to achieve turning and (iii) to faciliate walking in a straight line. We have never found CC lesions to restrict the range of stepping frequencies available to a fly. Mosaic analyses placed the foci of the impairments found in some lines with aberrant CC in the trunk.
The new line C31 exemplifies the importance of the CC for walking in a straight line. The flies, affected in an apparently unknown gene at 1-23cM, are impaired in three out of four CC-neuropilar regions and by the same mutation in the thoracical ganglion. When the defective gene is expressed unilaterally throughout the fly, the mosaic individuals continuously turn to the mutated side even when approaching a landmark. The tendency to turn is not observed in unilaterally thorax-defective mosaics with intact brains nor in completely defective C31 flies. The finding suggests that an intact CC is capable of compensating for the different performances of a defective and a normal body side. A C31-impaired brain, however, can no longer balance existing differences.
In a second line of evidence we show that the protocerebral bridge within the CC is involved in the adjustment of step lengths to optimize walking speed and probably also to achieve turning. Corresponding severe walking impairments in the mutant no-bridgeKS49 (Strauss et al. 1992 J Neurogenet 8:125-55) are paralleled by C141, central-complexKS181, and ocelliless1 (Leng and Strauss, this issue), all lines with disruptions of the protocerebral bridge. Mosaic studies have shown a full correlation of stride length with the state of the protocerebral bridge. The overlapping behavioral and structural aberrations in four lines, all affected in different genes, make it highly unlikely that the focus for the defective stride lengths is close to but outside the CC.