Connecting brain to behaviour: a role for general purpose steering circuits in insect orientation?

Abstract

The lateral accessory lobes (LALs), paired structures that are homologous among all insect species, have been well studied for their role in pheromone tracking in silkmoths and phonotaxis in crickets, where their outputs have been shown to correlate with observed motor activity. Further studies have shown more generally that the LALs are crucial both for an insect's ability to steer correctly and for organising the outputs of the descending pathways towards the motor centres. In this context, we propose a framework by which the LALs may be generally involved in generating steering commands across a variety of insects and behaviours. Across different behaviours, we see that the LAL is involved in generating two kinds of steering: (1) search behaviours and (2) targeted steering driven by direct sensory information. Search behaviours are generated when the current behaviourally relevant cues are not available, and a well-described LAL subnetwork produces activity which increases sampling of the environment. We propose that, when behaviourally relevant cues are available, the LALs may integrate orientation information from several sensory modalities, thus leading to a collective output for steering driven by those cues. These steering commands are then sent to the motor centres, and an additional efference copy is sent back to the orientation-computing areas. In summary, we have taken known aspects of the neurophysiology and function of the insect LALs and generated a speculative framework that suggests how LALs might be involved in steering control for a variety of complex real-world behaviours in insects.

A decentralised neural model explaining optimal integration of navigational strategies in insects

“…Follow-on neuroanatomically constrained modelling of the optic lobes presents the most obvious extension of this work allowing the neural pathway from sensory input to motor output signal to be mapped in detail. Conversely, modelling the conversion of direction signals into behaviour via motor generating mechanisms such as central pattern generators (see Steinbeck et al, 2020 ) will then allow closure of the sensory-motor loop.…”

Impact of central complex lesions on visual orientation in ants: Turning behaviour, but not the overall movement direction, is disrupted

“…It has previously been suggested that visual control of orientation in wood ants involves ‘correction points’ that are synchronised with the underlying path ‘wiggle’ or sinuosity (Lent et al 2010; Collett et al 2014). This suggest that there may be some independence between the control of underlying path sinuosity (perhaps from the lateral accessory lobes; (Steinbeck et al 2020)) and of visual corrections. Lateralised lesions in ants might not therefore knock-out the control of all turns in one direction but might diminish the visual control of those turns.…”

A projectome of the bumblebee central complex

“…PFL neurons relay signals to descending neurons in the lateral accessory lobes (LAL), making them likely candidates for cells which propagate steering or other motor commands to the ventral nerve cord (VNC) (Figure 7; Figure 8; Stone et al, 2017;Steinbeck et al, 2020;Rayshubskiy et al, 2020;Hulse et al, 2020). Connectomic analysis of the fly CX revealed the presence of three types of PFL neurons that differ in their PB-FB projection offset and downstream partners.…”