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Development of the circuits in the locust brain for the early detection and avoidance of looming objects

Final Report Summary - NEURAL DEVELOPMENT (Development of the circuits in the locust brain for the early detection and avoidance of looming objects.)

The visual detection of approaching stimuli is crucial in all stages of an animal´s life since it is involved in vital behaviours such as prey capture, collision-avoidance and predator escape responses. For example, human babies of only 6 days old already display evasive responses to the approach of an object. Therefore, the circuitries involved in looming detection should mature early in life although their development has not been specifically studied. Locusts have been extensively used to reveal the neural circuits and mechanisms involved in sensing looming stimuli and triggering visually-evoked evasive actions, making them ideal subjects to investigate its development. Inside their brains is the LGMD1 (usually referred as LGMD, lobula giant movement detector) neuron which selectively responds to approaching stimuli and provides information that eventually reaches motor centres commanding evasive responses like jumping and emergency glides. Recent evidence suggests that there must be other looming-sensitive neurons involved in triggering such responses although their identity is still uncertain. The LGMD2 neuron has been seldom studied but shares many response properties with the LGMD1 and thus is a valid candidate. Until now, most research has focussed on last moment reactions displayed just before collision. In this project, we analysed escape behaviours on the ground, particularly the hiding response (a positioning behaviour in which locusts sitting on branches tend to hide from an approaching stimulus by moving behind the object), that require more time to prepare and thus involve detection of predators at a longer range. Unveiling the circuitry beneath this type of behaviour may enable the development of technologies in cars/vehicles for hazard detection over a longer range.
This project was the concluding (return) phase of an International Incoming Fellowship (No: 236208, Development of the circuits in the locust brain for the early detection and avoidance of looming objects). In this project, we described the anatomy and ultrastructure of the synaptic connections of both LGMD neurons during all stages of the postembryonic development of Locusta migratoria. We also analysed changes and constancies witnessed during ontogeny in escape behaviours triggered by approaching stimuli, specially focussing on the hiding response. Our data suggest the involvement of the LGMD2 in such behaviour.
Our principal findings were:
1) We discovered that locusts were able to perform the hiding response in all developmental stages (even in 1-day-old first instars) implying that the neural pathway involved matures early in development (Sztarker and Rind, submitted).
2) We described, for the first time in juvenile instars the 3D structure of the LGMD1 and LGMD2, two key neurons for the detection of stimuli moving in an approaching pathway (see figures attached for examples). The overall shape (outline) of LGMD1 and LGMD2 was similar in all instars. Nonetheless, trees become bigger and more complex as locusts grow when considering the total length, the number of segments present in the tree, the branching pattern and the highest branch order. When comparing the development of the two neurons it seems like the LGMD2 matures faster, being the trees of the LGMD2 in 1st instars more complex than those of the LGMD1 (Sztarker and Rind, submitted).
3) We found that both LGMD1 and LGMD2 have mature synapses already at the earliest stage of development (in newly hatched 1st instars) and they already show the same the functional organisation as the adult (Sztarker and Rind, in preparation).
4) We proved that the LGMD1 of the 1st instars are already functional detectors of approaching stimuli. Our physiological recordings of DCMD axon spikes reveal that at the time of hatching the neurons already respond selectively to objects approaching the locust and they discriminate between different stimulus approach speeds with differences in spike frequency. Nonetheless, we observed that the selectivity (i.e. the performance in discriminating approaching from receding stimuli) improves as the locust goes through successive moults (Simmons et al, 2013).
5) By using computer-generated stimuli that were programmed following the response preferences of the LGMD2 but not those of the LGMD1 to trigger hiding responses, we established the LGMD2 as the candidate neuron involved in triggering the hiding response (Sztarker and Rind, submitted).

In summary, we made significant advances towards the originally planned objectives and are expecting to be able to incorporate our finding into biologically inspired circuits.