Abstract

Honeybees organize a sophisticated society, and the workers transmit information about the location of food sources using a symbolic dance, known as ‘dance communication’. Recent studies indicate that workers integrate sensory information during foraging flight for dance communication. The neural mechanisms that account for this remarkable ability are, however, unknown. In the present study, we established a novel method to visualize neural activity in the honeybee brain using a novel immediate early gene, kakusei, as a marker of neural activity. The kakusei transcript was localized in the nuclei of brain neurons and did not encode an open reading frame, suggesting that it functions as a non-coding nuclear RNA. Using this method, we show that neural activity of a mushroom body neuron subtype, the small-type Kenyon cells, is prominently increased in the brains of dancer and forager honeybees. In contrast, the neural activity of the two mushroom body neuron subtypes, the small-and large-type Kenyon cells, is increased in the brains of re-orienting workers, which memorize their hive location during re-orienting flights. These findings demonstrate that the small-type Kenyon cell-preferential activity is associated with foraging behavior, suggesting its involvement in information integration during foraging flight, which is an essential basis for dance communication.

Highlights

  • A variety of animals, from nematode to human, show social behavior [1,2]

  • We identified a novel immediate early genes (IEGs) that can be used as a neural activity marker and found that the neural activity of a mushroom body (MB) neuron subtype is preferentially increased in foraging honeybees, suggesting its involvement in information integration during foraging flight

  • To evoke strong neural activity in the brain, seizures were induced by awakening workers from ice-cold induced anesthesia, because some of the IEGs were identified by inducing seizures in the animals [16,17]

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Summary

Introduction

A variety of animals, from nematode to human, show social behavior [1,2]. The social behaviors allow for individuals to create an entity greater than the sum of the individuals and provide the key to successful adaptation to the environment. One of the most striking features of the highly-ordered animal society is the ability to share information among individuals. Higher communicative ability is a fundamental basis that enables animals to maintain a more evolved society [3]. Honeybees (Apis mellifera L.) organize a highly-ordered society and have a sophisticated communicative ability known as the ‘dance communication’ [4,5,6,7]. During foraging flights, worker honeybees integrate the incoming sensory information: they estimate the distance of food sources based on the amount of optic flow they perceive, and direction based on the position of the sun [5,8,9], which are the essential bases for the expression of dance communication. There is a considerable amount of research concerning the sensory basis of these remarkable abilities [8,9,10,11], almost nothing is known about the underlying neural mechanisms

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