Relationship between the Phases of Sensory and Motor Activity during a Looming-Evoked Multistage Escape Behavior

Abstract

The firing patterns of visual neurons tracking approaching objects need to be translated into appropriate motor activation sequences to generate escape behaviors. Locusts possess an identified neuron highly sensitive to approaching objects (looming stimuli), thought to play an important role in collision avoidance through its motor projections. To study how the activity of this neuron relates to escape behaviors, we monitored jumps evoked by looming stimuli in freely behaving animals. By comparing electrophysiological and highspeed video recordings, we found that the initial preparatory phase of jumps occurs on average during the rising phase of the firing rate of the looming-sensitive neuron. The coactivation period of leg flexors and extensors, which is used to store the energy required for the jump, coincides with the timing of the peak firing rate of the neuron. The final preparatory phase occurs after the peak and takeoff happens when the firing rate of the looming-sensitive neuron has decayed to Ͻ10% of its peak. Both the initial and the final preparatory phases and takeoff are triggered when the approaching object crosses successive threshold angular sizes on the animal's retina. Our results therefore suggest that distinct phases of the firing patterns of individual sensory neurons may actively contribute to distinct phases of complex, multistage motor behaviors.

Collision-avoidance behaviors of minimally restrained flying locusts to looming stimuli

“…At the end of the encounter epoch, the last frame of this stimulus was kept for an additional 1.15s before the screen returned to its background luminance level. Instead of a real approaching object, the looming stimulus employed in these experiments reproduced the expanding shadow of a black square on a white background (Fotowat and Gabbiani, 2007;. The scotopic luminance of the white background was 2760cdm -2 and that of the black square 3.32cdm -2 .…”

“…All experiments were performed with l/|v| equal to 40ms. This value was selected because it was in the range of values yielding high escape probabilities in earlier jump escape experiments (Fotowat and Gabbiani, 2007). Higher l/|v| values were impractical because of limitations imposed by the camera memory.…”

“…The neural circuits mediating collision-avoidance behaviors are well defined in S. americana, as well as in the closely related species Schistocerca gregaria (desert locust) (Sword, 2003) and Locusta migratoria (migratory locust) for which many extensive investigations have been carried out (for review, see . The mechanisms underlying jump escape behaviors to looming stimuli, the two-dimensional (2D) expanding shadows associated with objects approaching on a collision course with the animal, have been most studied (Fotowat and Gabbiani, 2007;Santer et al, 2005b;Santer et al, 2008). The lobula giant movement detector (LGMD)/descending contralateral movement detector (DCMD) pathway is thought to underlie these behaviors, based on extensive work carried out since its initial anatomical and electrophysiological characterization (O'Shea and Rowell, 1974;O'Shea and Williams, 1974;Schlotterer, 1977;Rind and Simmons, 1992;Hatsopoulos et al, 1995).…”

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).…”

“…They play roles in triggering behavioural responses to approaching objects (Fotowat and Gabbiani, 2007;Santer et al, 2006;Santer et al, 2008). Individual neurons in other species have also been shown to respond to and trigger responses to approaching objects, but the way in which selectivity for approaching stimuli arises has been most thoroughly investigated in the locust LGMD (de Vries and Clandinin, 2012;Dewell and Gabbiani, 2012;Oliva et al, 2007;Preuss et al, 2006).…”