Neural correlates to flight‐related density‐dependent phase characteristics in locusts

Abstract

Locust phase polymorphism is an extreme example of behavioral plasticity; in response to changes in population density, locusts dramatically alter their behavior. These changes in behavior facilitate the appearance of various morphological and physiological phase characteristics. One of the principal behavioral changes is the more intense flight behavior and improved flight performance of gregarious locusts compared to solitary ones. Surprisingly, the neurophysiological basis of the behavioral phase characteristics has received little attention. Here we present density-dependent differences in flight-related sensory and central neural elements in the desert locust. Using techniques already established for gregarious locusts, we compared the response of locusts of both phases to controlled wind stimuli. Gregarious locusts demonstrated a lower threshold for wind-induced flight initiation. Wind-induced spiking activity in the locust tritocerebral commissure giants (TCG, a pair of identified interneurons that relay input from head hair receptors to thoracic motor centers) was found to be weaker in solitary locusts compared to gregarious ones. The solitary locusts' TCG also demonstrated much stronger spike frequency adaptation in response to wind stimuli. Although the number of forehead wind sensitive hairs was found to be larger in solitary locusts, the stimuli conveyed to their flight motor centers were weaker. The tritocerebral commissure dwarf (TCD) is an inhibitory flight-related interneuron in the locust that responds to light stimuli. An increase in TCD spontaneous activity in dark conditions was significantly stronger in gregarious locusts than in solitary ones. Thus, phase-dependent differences in the activity of flight-related interneurons reflect behavioral phase characteristics.

The locust foraging gene

“…These included all reported differences in morphometric ratios, coloration and pattern, and development. Further, recently reported neurophysiological differences (Fuchs et al, 2003) and behavioral differences (Geva et al, 2010) are also very robust and consistent.…”

“…In locusts, gregarious animals are characterized by diurnal flight behavior, while solitary locusts fly at night. Fuchs et al (2003) describe an identified flight-related inhibitory interneuron, which is sensitive to illumination level, and show a remarkable and highly significant increase in activity during the dark but only when locusts are crowded locusts. Lastly, serotonin (5-hydroxtryptamine, 5HT) is both necessary and sufficient for locust phase transformation, with increasing levels of 5HT accompanying (and inducing) gregariousness (Anstey et al, 2009).…”

“…Recent findings have identified the primary sensory inputs inducing a densitydependent phase change in locusts . Other neurobiology research has characterized differences in sensory interneurons that mediate behavioral changes between the locust phases (e.g., wind-sensitive interneurons, Fuchs et al, 2003;visual interneurons, Matheson et al, 2004). In marked contrast, little has been achieved in the study of the molecular and genetic contributions to this phenomenon (see recent reviews in Simpson et al, 2005;Simpson and Sword, 2008;Pener and Simpson, 2009).…”

Epigenetics and locust life phase transitions

“…In contrast, the larger brains of gregarious locusts are more dedicated to the integration of sensory cues in higher level processing regions, which is thought to support their lifestyle as generalist foragers in dense, migratory swarms where competition among group members is high (Ott and Rogers, 2010). Other changes in brain functioning situate at the level of circuit activity and function (Ayali et al, 2004; Blackburn et al, 2010; Burrows et al, 2011;Fuchs et al, 2003). For example, gregarious L. migratoria show reduced habituation of interneuron activity in response to approaching objects.…”

Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust

“…There are also clear differences in specific neuronal circuits and muscular systems between the two extreme locust phases that can be related to these differences in behaviour (Matheson et al, , 2004Blackburn et al, 2003;Fuchs et al, 2003). The neuro-hormonal mechanisms that drive and maintain phase change, however, remain largely unknown (Pener, 1991;Pener and Yerulshami, 1998;Breuer et al, 2003).…”