Abstract

Serotonin is a neurochemical with evolutionarily conserved roles in orchestrating nervous system function and behavioural plasticity. A dramatic example is the rapid transformation of desert locusts from cryptic asocial animals into gregarious crop pests that occurs when drought forces them to accumulate on dwindling resources, triggering a profound alteration of behaviour within just a few hours. The onset of crowding induces a surge in serotonin within their thoracic ganglia that is sufficient and necessary to induce the switch from solitarious to gregarious behaviour. To identify the neurons responsible, we have analysed how acute exposure to three gregarizing stimuli—crowding, touching the hind legs or seeing and smelling other locusts—and prolonged group living affect the expression of serotonin in individual neurons in the thoracic ganglia. Quantitative analysis of cell body immunofluorescence revealed three classes of neurons with distinct expressional responses. All ganglia contained neurons that responded to multiple gregarizing stimuli with increased expression. A second class showed increased expression only in response to intense visual and olfactory stimuli from conspecifics. Prolonged group living affected a third and entirely different set of neurons, revealing a two-tiered role of the serotonergic system as both initiator and substrate of socially induced plasticity. This demonstrates the critical importance of ontogenetic time for understanding the function of serotonin in the reorganization of behaviour.

Highlights

  • Serotonin (5-hydroxytryptamine) is a monoamine neurotransmitter, neuromodulator and neurohormone that has a prominent and evolutionarily conserved role in the control and regulation of a wide range of behaviours [1,2]

  • Serotonin immunofluorescence staining revealed a small population of neuronal somata in each of the three thoracic ganglia and densely interwoven neuronal processes that ramified throughout the neuropiles

  • These processes arose from a mixture of interneurons with somata in the thoracic ganglia, intersegmental interneurons with somata in other parts of the central nervous system (CNS), and some incoming sensory afferents

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Summary

Introduction

Serotonin (5-hydroxytryptamine) is a monoamine neurotransmitter, neuromodulator and neurohormone that has a prominent and evolutionarily conserved role in the control and regulation of a wide range of behaviours [1,2]. The onset of exposure to gregarizing stimuli leads to a dramatic increase in the amount of serotonin in the thoracic ganglia but not in the brain, as measured by HPLC [30] (figure 1a), which is sufficient and necessary to induce the initial transformation from solitarious to gregarious behaviour [25,26]. The effects of treatment on individual neurons were analysed by comparing the intensities of staining in the long-term gregarious, crowded, touch and sight þ smell stimulated locusts in independent contrasts against the long-term solitarious locusts (electronic supplementary material, tables S1 – S3).

Results
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Discussion
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