Which neuronal processes are modulated to attenuate the ‘drive’ for walking? Our recent data indicates that the behavioral manipulation of cockroaches is achieved by, at least, venom-induced inhibition of neuronal activity in the sub-esophageal ganglion (SEG). This small region in the cerebral CNS has been previously suggested to tonically regulate motor behavior through descending interneurons which, in turn, synapse onto thoracic premotor and motor circuitries ().9–12
We found that spontaneous and stimulus-evoked neuronal activity in the SEG is decreased in stung cockroaches, and that experimental injections of venom or local anesthetics into the SEG perturb walking initiation in normal cockroaches. In marked contrast, experimental injection of venom or anesthetics into a different part of the cerebral ganglia, namely the supraesophageal ganglion (SupEG), produces the opposite effect and promotes walking, even in the absence of external stimuli.5,13
These results are in agreement with previous lesions experiments (reviewed in ref. 12
) and suggest that the motor pattern generator (PG) responsible for the expression of walking-related behaviors receive, simultaneously, tonic permissive inputs from the SEG and inhibitory inputs from the SupEG (). The same appears to be true for other PGs as well: the flying PG, for instance, was also found to receive tonic antagonistic inputs from the SEG and SupEG, although here the SEG inhibits the PG, while the SupEG is permissive.12
Thus, the antagonistic interplay between descending inputs appears to regulate, either directly or indirectly through thoracic neuromodulatory neurons (such as the Dorsal or Ventral Unpaired Median neurons), the excitability of the different thoracic PGs. Internal and external sensory inputs, which represent different aspects of the animal in its environment, are thus expected to selectively modify the fine balance between permissive and inhibitory inputs descending to a specific PG, thereby priming the appropriate PG to favor the expression of one motor behavior over others. This, in turn, would determine the propensity of expression of different behaviors (such as walking or flying), and thus the ‘motivation’ of the animal to produce these behaviors. Several investigations suggest that the Central Body Complex and Mushroom Bodies, two distinct neuropiles in the SupEG which are involved in sensory integration and pre-motor processing,14–18
might also take part in the ongoing regulation of locomotion. Interestingly, when venom of the Jewel Wasp is traced in the cerebral ganglia of stung cockroaches, a large amount of venom is found in and around these SupEG neuropiles.19
Hence, we are currently investigating the involvement of these neuropiles in the ‘zombification’ of cockroaches by the Jewel Wasp (reviewed in ref. 20
To conclude, we hope that by investigating the neuronal basis of such parasite-induced alterations of host behavior, we might further our understanding of the neurobiology of the selection and initiation of behaviors and the associated neural mechanisms underlying changes in behavioral spontaneity. Our results indicate a mechanism which might cut through phylogenetic borders and could form the biological substrate for what we humans experience as “free will”.