Sensory processing and decision making in a social context : From odors to swarm motion in insects

Abstract

‘They covered the ground until it was black. They consumed everything left after the hail - every plant in the fields and all the fruit on the trees...’ (Exodus 10). The plague of locusts was the eighth disaster God sent to punish the Pharaoh. Nevertheless, despite millennia of progress, in the age of genetic engineering and space exploration, humanity still struggles to control the recurring devastation by locust swarms, which keep on threatening nearly 10% of the global human population during outbreaks. Another creature thriving between us and resisting humanity’s best efforts to eradicate it is the cockroach - an evolutionary survivor that has outlasted most species for over 300 million years. Locusts and cockroaches exemplify how simple individual actions can scale into detrimental, yet extremely fascinating complex collective dynamics, which enable the survival of the two species in ever fluctuating environments. The neurophysiological processing of external stimuli through sensory pathways allows those two non-model organisms to successfully navigate their surroundings, which, most often, include conspecifics. Social cues have the capability of triggering drastic changes in behavior and of influencing the perception of other non-social cues. Thus far, neuroscience has paid little attention to the neuronal mechanisms underlying natural social influences on behavior, traditionally focusing on preparations of tethered, isolated individuals under controlled laboratory conditions. During my PhD research, I explored how key ecological behaviors during decision-making are adapted and modulated under varying social contexts and how this is reflected in the sensory perception and information processing along specific neuronal pathways. The present cumulative dissertation aims to better understand the neuroethological foundations underlying social-enhancement or modification of an individual’s sensory perception. It comprises a general introduction and discussion, framing three consecutive publications, each presented as a separate chapter and introduced with a chapter summary. In Chapter 1, we investigated the modulatory impact of social cues during shelter selection in American cockroaches. Combining binary choice experiments and in-vivo calcium imaging, we found a socially induced preference shift, corresponding to an altered, early-stage neuronal coding. This neuronal modification and induced behavioral switch could help regulate resource 2 use by reducing attraction to previously exploited sites, potentially promoting the exploration of new resources. Building on the understanding of how social cues can reshape individual biases, and inspired by field work on locusts in Africa, Chapter 2 moves on to the foraging decisions of locusts, which demonstrate a remarkable and fascinating form of social plasticity. We studied how sensory integration, with and without a social context, influences foraging decisions by combining behavioral assays, Bayesian modeling, and neural imaging. By means of the first applications of in-vivo calcium imaging in a large proportion of projection neurons in desert locusts, the neuronal analysis revealed that gregarious locusts, unlike solitarious individuals, exhibit modulations originating in the first olfactory processing center. We assume that this effect enhances food detection in the distractive swarm environment. In accordance with our findings in Chapter 1, this study corroborates the result that the social context can reshape or override individual preferences, emphasizing the neuronal influence of groups on decision-making. Driven by the spectacular swarming behavior of locusts, which we witnessed during a major outbreak in Africa, Chapter 3 shifts the focus from how the social context influences individual choices and neural firing, to how socially induced individuals coordinate their coherent movement so as to form the foundation of collective swarm behavior. Through field experiments, virtual reality, quantitative behavioral analyses, and modeling approaches, we scrutinized the rules governing synchronized motion within large juvenile locust groups. Our findings reveal a sophisticated, self-reflective and vision-based mechanism underlying swarm alignment during motion. Together, the three studies provide new insights into the dynamic interplay between neural mechanisms, social influence, and swarm coordination, with broader implications for fundamental neuroscience and behavioral biology. I hope that our work, including the development of technical methods, can contribute to elaborating targeted pest management strategies in the future - a crucial step for combatting human starvation while also protecting countless ecologically relevant and threatened insect species from broad-spectrum insecticides.