Multiplexing of Motor Information in the Discharge of a Collision Detecting Neuron during Escape Behaviors

Abstract

Locusts possess an identified neuron, the descending contralateral movement detector (DCMD), conveying visual information about impending collision from the brain to thoracic motor centers. We built a telemetry system to simultaneously record, in freely behaving animals, the activity of the DCMD and of motoneurons involved in jump execution. Co-contraction of antagonistic leg muscles, a required preparatory phase, was triggered after the DCMD firing rate crossed a threshold. Thereafter, the number of DCMD spikes predicted precisely motoneuron activity and jump occurrence. Additionally, the time of DCMD peak firing rate predicted that of jump. Ablation experiments suggest that the DCMD, together with a nearly identical ipsilateral descending neuron, is responsible for the timely execution of the escape. Thus, three distinct features that are multiplexed in a single neuron’s sensory response to impending collision – firing rate threshold, peak firing time, and spike count – likely control three distinct motor aspects of escape behaviors.

Looming detection by identified visual interneurons during larval development of the locust,Locusta migratoria

“…In adults, one function for the DCMD is to trigger a diving glide during flight, which might enable evasion from capture by predatory birds or collision with other locusts in a swarm (Santer et al, 2012;Santer et al, 2006). It also plays a role in triggering jumps (Fotowat and Gabbiani, 2007;Santer et al, 2008), and recent evidence suggests that it plays distinct roles during different phases in preparing for and performing a jump (Fotowat et al, 2011). The DCMD acts in concert with other interneurons in the control of jumps, some of which respond to approaching stimuli (Gray et al, 2010;Simmons and Rind, 1997).…”

Head and body stabilization in blowflies walking on differently structured substrates

“…One possible approach to investigate this issue may be to record the activity of optic-flow-processing neurons during stimulation with reconstructed optic flow as perceived by freely walking blowflies, as has already been done for flying flies Karmeier et al, 2006). Because behavioral activity and, in particular, locomotion can affect the response properties of these neurons to some extent (Jung et al, 2011;Chiappe et al, 2010;Maimon et al, 2010;Rosner et al, 2010), it would be desirable to make neuronal recordings in the behaving fly as has recently been successfully accomplished in the much larger locust (Fotowat et al, 2011). With this new technique, it might be possible to estimate what spatial information can be extracted from optic-flow-processing neurons during free walking.…”

Bilateral flight muscle activity predicts wing kinematics and 3-dimensional body orientation of locusts responding to looming objects

“…Generating appropriate aerodynamic forces while staying aloft requires rapid detection and integration of salient visual cues. Animals have evolved neural circuitry adapted to preferentially detect visual edge expansion of looming stimuli and respond accordingly by generating emergency escape behaviours [for example, frogs (Nakagawa and Hongjian, 2010), cats (Liu et al, 2011), pigeons (Wang and Frost, 1992), crabs (Oliva et al, 2007;Sztarker and Tomsic, 2008) and insects such as flies (Holmqvist and Srinivasan, 1991;Fotowat et al, 2009) and locusts (Robertson and Reye, 1992;Robertson and Johnson, 1993;Gray et al, 2001;Santer et al, 2005;Simmons et al, 2010;Fotowat et al, 2011;Chan and Gabbiani, 2013)]. …”