Identifying neural substrates of competitive interactions and sequence transitions during mechanosensory responses in Drosophila

Abstract

Nervous systems have the ability to select appropriate actions and action sequences in response to sensory cues. The circuit mechanisms by which nervous systems achieve choice, stability and transitions between behaviors are still incompletely understood. To identify neurons and brain areas involved in controlling these processes, we combined a large-scale neuronal inactivation screen with automated action detection in response to a mechanosensory cue in Drosophila larva. We analyzed behaviors from 2.9x10 5 larvae and identified 66 candidate lines for mechanosensory responses out of which 25 for competitive interactions between actions. We further characterize in detail the neurons in these lines and analyzed their connectivity using electron microscopy. We found the neurons in the mechanosensory network are located in different regions of the nervous system consistent with a distributed model of sensorimotor decision-making. These findings provide the basis for understanding how selection and transition between behaviors are controlled by the nervous system.

Useful road maps: studying Drosophila larva’s central nervous system with the help of connectomics

“…In addition, the larva has a rich behavioral repertoire, exhibiting a range of distinct actions and sequences [ 6 , 8 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 ] ( Figure 1 iv ) and is capable of robust associative learning [ 16 , 17 , 18 , 43 , 44 , 45 , 46 , 47 , 48 , 49 ]. Automatic tracking of individual larvae and behavioral categorization greatly facilitates relating the structure of larval circuits to their function [ 6 , 8 , 13 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 39 , 49 , 50 ]. High-throughput behavioral inactivation and activation screens allow identifying neurons promoting or repressing specific actions or computations [ 8 , 33 , 36 , 41 , 50 , 51 ].…”

“…Automatic tracking of individual larvae and behavioral categorization greatly facilitates relating the structure of larval circuits to their function [ 6 , 8 , 13 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 39 , 49 , 50 ]. High-throughput behavioral inactivation and activation screens allow identifying neurons promoting or repressing specific actions or computations [ 8 , 33 , 36 , 41 , 50 , 51 ].…”

“…Likely, the VNC and SEZ regions are thus the last steps where conflict for different types of actions may be resolved. Reconstructing the full pathways for different behavioral drives all the way from a comprehensive set of sensory inputs to a comprehensive set of command neurons will allow identifying their sites of interactions and potential conflict resolution; this may result in refining our views of the processes defined as action selection or decision [ 8 , 36 ].…”

A physical theory of movement in small animals

“…The estimated midline is given by a set of equally spaced points, allowing characterisation of transverse bending but not axial compression/expansion. Larval midlines and contours were used to score bouts of rolling behaviour, as described elsewhere [27]. Larvae that were tracked for fewer than 5 seconds, or travelled less than one body length in distance, were rejected.…”

“…As well as extensive behavioural data, there is currently a concerted effort to map the neural connectome of the larva, and to link observed neural anatomy and dynamics to behaviour [16][17][18][19][20][21][22][23][24][25][26][27]. Moreover, recent modelling studies have already explored the importance of biomechanics in understanding the animal's crawling (in 1 spatial dimension) [28][29][30][31] and substrate exploration/taxis behaviours (in 2 spatial dimensions) [30,32,33], emphasising the crucial role that sensory feedback, which conveys some measurement of the physical state of the animal to its nervous system, plays during behaviour [28][29][30][31]33].…”