Escapes with and without preparation: The neuroethology of visual startle in locusts

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

“…Moreover, we describe, for the first time, that the relative timing and spike numbers in a flight depressor muscle (m97) can predict wing kinematics and 3-dimensional body orientation in locusts responding to looming stimuli. Studying behavioural responses to looming stimuli in minimally restrained locusts, as described here (see also Chan and Gabbiani, 2013), provides a more natural representation of flight compared with experiments using rigidly tethered animals (Hedwig and Becher, 1998;Robertson and Reye, 1992;Robertson and Johnson, 1993;Gray et al, 2001;Santer et al, 2005;Santer et al, 2006;Simmons et al, 2010;Ribak et al, 2012). Using a combination of loose and more restrictive tight tethering, Chan and Gabbiani (Chan and Gabbiani, 2013) described wing kinematics and body positions in Schistocerca americana, which fly relatively short distances compared with the much longer flight durations of L. migratoria.…”

“…Rigidly tethered flying locusts consistently respond to lateral looming stimuli by interrupting flight and turning away from or toward the stimulus (Robertson and Johnson, 1993;Dawson et al, 1997;Robertson et al, 1996;Dawson et al, 2004b) and turning primarily away from the stimulus or performing a glide as a last ditch response (Robertson and Reye, 1992;Santer et al, 2005;Santer et al, 2006;Rind et al, 2008;Simmons et al, 2010;Santer et al, 2012;Ribak et al, 2012). We found that most animals turned as an initial response to the looming stimulus (33% turned left, 28% turned right), while 39% of the animals glided.…”

“…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)]. …”

“…Locusts respond to looming stimuli by performing subtle movements of their appendages to hide behind a blade of grass (Hassenstein and Hustert, 1999), kicking and jumping (Burrows and Rowell, 1973;Burrows, 1995), or turning and gliding during flight (Robertson and Reye, 1992;Robertson and Johnson, 1993;Gray et al, 2001;Santer et al, 2005;Simmons et al, 2010;Chan and Gabbiani, 2013). While flying in dense swarms and avoiding collisions with conspecifics, locusts must also escape potential aerial predators (Waloff, 1972;Santer et al, 2012).…”

“…This type of aerobatic control is largely influenced by the locust's visual system (Gray et al, 2001;Santer et al, 2005;Santer et al, 2006), which contains multiple looming-sensitive neurons that synapse with flight motor neurons in the thorax (Simmons, 1980). To date, flight muscle activity, wing kinematics and aerodynamic forces recorded during a collision avoidance behaviour have been measured from rigidly tethered locusts flying in open-loop conditions (Robertson and Reye, 1992;Robertson and Johnson, 1993;Hedwig and Becher, 1998;Gray et al, 2001;Santer et al, 2005;Santer et al, 2006;Simmons et al, 2010;Ribak et al, 2012), which introduces potentially confounding artefacts (Robertson and Reye, 1992;Dawson et al, 2004a;Shoemaker and Robertson, 1998). However, loosely tethered flying locusts are capable of changing orientation in response to looming stimuli within a single wing beat (Mohr and Gray, 2003).…”