A spike-timing mechanism for action selection

Abstract

We discovered a bimodal behavior in the genetically tractable organism Drosophila melanogaster that allowed us to directly probe the neural mechanisms of an action selection process. When confronted by a predator-mimicking looming stimulus, a fly responds with either a long-duration escape behavior sequence that initiates stable flight or a distinct, short-duration sequence that sacrifices flight stability for speed. Intracellular recording of the descending giant fiber (GF) interneuron during head-fixed escape revealed that GF spike timing relative to parallel circuits for escape actions determined which of the two behavioral responses was elicited. The process was well described by a simple model in which the GF circuit has a higher activation threshold than the parallel circuits, but can override ongoing behavior to force a short takeoff. Our findings suggest a neural mechanism for action selection in which relative activation timing of parallel circuits creates the appropriate motor output.

Mechanics of the thorax in flies

“…During take-off, flies use two different pathways to initiate flight (Trimarchi and Schneiderman, 1995a;von Reyn et al, 2014). During slow, voluntary take-off, the two wings lift together and start flapping just as the fly jumps off.…”

The use of computational modeling to link sensory processing with behavior in Drosophila

“…The genetic model organism Drosophila melanogaster exhibits a range of robust and complex behaviors such as acoustic communication during courtship (Coen et al 2014;Clemens et al 2015a;Coen et al 2016), detection and integration of multisensory cues to locate food sources (van Breugel and Dickinson 2014;Bell and Wilson 2016), visually guided flight control (Clark et al 2011;Aptekar et al 2012;de Vries and Clandinin 2012;Silies et al 2014), and avoidance of threats (Reyn et al 2014). Recording Drosophila behaviors can be done in high-throughput, and its numerically compact and largely hardwired nervous system facilitates identifying the underlying neurons.…”

“…This can also be applied to behavioral events (in lieu of spikes) like the onset of an escape behavior (Reyn et al 2014) or the individual pulses of fly song (Coen et al 2016). A simple generalization enables applying the STA approach to continuous outputs like neuronal calcium levels or the amplitude of the animal's communication signal (Kato et al 2014;Coen et al 2016).…”

Hearing in Drosophila

“…10.8.3 , the GF and the AMMC-A1 neurons form the GF system. The GF system of fruit fl ies mediates a short latency jump-fl ight response through the activation of motor neurons in the thorax (Allen et al 2006 ;von Reyn et al 2014 ). The GF is a pair of descending neurons activated by either visual looming stimuli or sound (Tootoonian et al 2012 ;von Reyn et al 2014 ).…”