Immediate and punitive impact of mechanosensory disturbance on olfactory behaviour of larval Drosophila

Abstract

The ability to respond to and to learn about mechanosensory disturbance is widespread among animals. Using Drosophila larvae, we describe how the frequency of mechanosensory disturbance (‘buzz’) affects three aspects of behaviour: free locomotion, innate olfactory preference, and potency as a punishment. We report that (i) during 2–3 seconds after buzz onset the larvae slowed down and then turned, arguably to escape this situation; this was seen for buzz frequencies of 10, 100, and 1000 Hz, (ii) innate olfactory preference was reduced when tested in the presence of the buzz; this effect was strongest for the 100 Hz frequency, (iii) after odour-buzz associative training, we observed escape from the buzz-associated odour; this effect was apparent for 10 and 100, but not for 1000 Hz. We discuss the multiple behavioural effects of mechanosensation and stress that the immediate effects on locomotion and the impact as punishment differ in their frequency-dependence. Similar dissociations between immediate, reflexive behavioural effects and reinforcement potency were previously reported for sweet, salty and bitter tastants. It should be interesting to see how these features map onto the organization of sensory, ascending pathways.

One-trial learning in larval Drosophila

“…In neither case, however, have systematic analyses of one-trial associative learning been reported. Rather, analyses of associative learning in the larva have so far focused almost exclusively on three-trial conditioning, whether for various sugars (Scherer et al 2003;Schipanski et al 2008;Rohwedder et al 2012) and amino acids as taste rewards (Schleyer et al 2015a), for optogenetically induced reward learning through the activation of subsets of dopaminergic neurons (Saumweber et al 2018), for punishment by substrate vibration (Eschbach et al 2011;Saumweber et al 2014) or electric shocks (Pauls et al 2010), or for quinine as taste punishment (Gerber and Hendel 2006;El-Keredy et al 2012;Apostolopoulou et al 2014). Only for salt, that is high concentrations of sodium chloride, have analyses of three-trial learning (Gerber and Hendel 2006;Niewalda et al 2008) recently been complemented by an experiment reporting associative memory after just one training trial (Widmann et al 2016; loc.…”

The Ol1mpiad: concordance of behavioural faculties of stage 1 and stage 3Drosophilalarvae

“…To measure the locomotor changes by mechanosensory disturbance, we used the 'buzz' set-up described in Eschbach et al 2011and Saumweber et al (2014), with minor changes to accommodate the small size of L1. Specifically, (i) a higher-resolution camera (Basler ace acA2040-90umNIR, Ahrensburg, Germany), (ii) new, customwritten software, and (iii) agarose-filled Petri dishes of smaller diameter (90 mm) were used.…”

“…We measured translational run speed as well as the angular sideways speed of L1 and L3, both under baseline conditions and upon presentation of a disturbing mechanosensory 'buzz' stimulus (Eschbach et al, 2011;Saumweber et al, 2014). Under baseline conditions, translational run speed was about 4-fold lower in L1 than in L3, while angular speed was equal in the two stages (Fig.…”

Multisensory neural integration of chemical and mechanical signals

“…The adaptive advantage of this modulation might be to focus the worm on the immediate sensory challenges so that it is not distracted by less relevant mechanosensory input while it tries to escape adverse conditions. In a similar type of study with Drosophila larvae, mechanosensory disturbance − in the form of high frequency “buzzes,” perhaps reminiscent of the sound of parasitoid wasps − reduced behavioral responses to attractive odors .…”