Escape behavior and neuronal responses to looming stimuli in the crabChasmagnathus granulatus(Decapoda: Grapsidae)

Abstract

SUMMARY Behavioral responses to looming stimuli have been studied in many vertebrate and invertebrate species, but neurons sensitive to looming have been investigated in very few animals. In this paper we introduce a new experimental model using the crab Chasmagnathus granulatus, which allows investigation of the processes of looming detection and escape decision at both the behavioral and neuronal levels. By analyzing the escape response of the crab in a walking simulator device we show that: (i) a robust and reliable escape response can be elicited by computer-generated looming stimuli in all tested animals; (ii) parameters such as distance, speed, timing and directionality of the escape run, are easy to record and quantify precisely in the walking device; (iii) although the magnitude of escape varies between animals and stimulus presentations, the timing of the response is remarkably consistent and does not habituate at 3 min stimulus intervals. We then study the response of neurons from the brain of the crab by means of intracellular recordings in the intact animal and show that: (iv) two subclasses of previously identified movement detector neurons from the lobula (third optic neuropil) exhibit robust and reliable responses to the same looming stimuli that trigger the behavioral response; (v) the neurons respond to the object approach by increasing their rate of firing in a way that closely matches the dynamics of the image expansion. Finally, we compare the neuronal with the behavioral response showing that: (vi) differences in the neuronal responses to looming, receding or laterally moving stimuli closely reflect the behavioral differences to such stimuli; (vii) during looming, the crab starts to run soon after the looming-sensitive neurons begin to increase their firing rate. The increase in the running speed during stimulus approach faithfully follows the increment in the firing rate, until the moment of maximum stimulus expansion. Thereafter, the neurons abruptly stop firing and the animal immediately decelerates its run. The results are discussed in connection with studies of responses to looming stimuli in the locust.

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)]. …”

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

“…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). The LGMD has an extensive dendritic arbour in the lobula, through which it collects inputs from ommatidia over a wide area of the visual field (Krapp and Gabbiani, 2005).…”

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

“…Some animals have evolved fast motor circuits devoted to the generation of such behaviors, such as the giant fiber system in flies, the Mauthner cell in fish, or the lateral giant neurons of crayfish (Wyman et al, 1984;Edwards et al, 1999;Korn and Faber, 2005). Although much is known in these and in other systems about how escape behaviors are generated in response to abrupt stimuli such as mechanical disturbances, air puffs, or light flashes (Levi and Camhi, 2000;Fayyazuddin et al, 2006;Bhatt et al, 2007), we still know very little about how escape behaviors are generated in response to objects approaching on a collision course, as may be expected from potential predators (Yamamoto et al, 2003;Preuss et al, 2006;Santer et al, 2006;Oliva et al, 2007;Hammond and O'Shea, 2007).…”