Interneurons in the Honeybee Primary Auditory Center Responding to Waggle Dance-Like Vibration Pulses

Abstract

Female honeybees use the "waggle dance" to communicate the location of nectar sources to their hive mates. Distance information is encoded in the duration of the waggle phase (von Frisch, 1967). During the waggle phase, the dancer produces trains of vibration pulses, which are detected by the follower bees via Johnston's organ located on the antennae. To uncover the neural mechanisms underlying the encoding of distance information in the waggle dance follower, we investigated morphology, physiology, and immunohistochemistry of interneurons arborizing in the primary auditory center of the honeybee (). We identified major interneuron types, named DL-Int-1, DL-Int-2, and bilateral DL-dSEG-LP, that responded with different spiking patterns to vibration pulses applied to the antennae. Experimental and computational analyses suggest that inhibitory connection plays a role in encoding and processing the duration of vibration pulse trains in the primary auditory center of the honeybee. The waggle dance represents a form of symbolic communication used by honeybees to convey the location of food sources via species-specific sound. The brain mechanisms used to decipher this symbolic information are unknown. We examined interneurons in the honeybee primary auditory center and identified different neuron types with specific properties. The results of our computational analyses suggest that inhibitory connection plays a role in encoding waggle dance signals. Our results are critical for understanding how the honeybee deciphers information from the sound produced by the waggle dance and provide new insights regarding how common neural mechanisms are used by different species to achieve communication.

The mechanosensory‐motor apparatus of antennae in the Oleander hawk moth (Daphnis nerii, Lepidoptera)

“…Second, the observation that Böhm's bristles arbors terminate in the ipsilateral AMMC means that bilaterally coordinated antennal movements, such as those observed during initiation or maintenance of flight, must require as interneurons between left and right AMMCs to coordinate motor activity for both antennae. Bilateral interneurons which span across the dorsal lobes, sub‐oesophagal ganglia, lateral protocerebrum and posterior protocerebral lobe have been recently reported, for instance, in honeybees in the context of encoding specific parameters of the waggle dance, such as direction of food source (Ai et al, ). Detailed neuroanatomical studies are required to identify such neurons in other insects in the context of motor coordination.…”

Adaptations during maturation in an identified honeybee interneuron responsive to waggle dance vibration signals

“…Experiments were conducted on more than 300 bees for investigating neurons in the primary auditory center of the honeybee brain. Collected data included electrophysiological recordings and laser scanning microscopy images, which were stored in a database and classified into multiple neuron groups based on electrophysiological and morphological characteristics (see Table 1, Ai et al 2017). In the current study, we used DL-Int-1 data from the database belonging to honeybees of two stages of maturation: Newly emerged adults (age 1-3 days): female honeybees shortly after emerging from their cell in the hive.…”

“…The experimental procedure for generating LSM image stacks and electrophysiological response traces from honeybee vibration-sensitive interneurons has been presented in detail in Ai et al (2017) and we describe it here briefly. After immobilization and head fixing using bee’s wax, the frontal surface of the honeybee brain was exposed by cutting away a small rectangular window between the compound eyes.…”

“…More than ten groups of interneurons belonging to three categories have been identified and characterized in these regions (Ai et al 2009; Ai 2010; Ai 2013; Ai et al 2017)) and have been shown to respond to air-borne vibration pulses similar to those produced during the waggle dance (Ai et al 2017). In particular, a group of GABAergic interneurons called DL-Int-1 has been studied intensively and has been characterized in detail (Ai et al 2009; Ai 2013; Ai et al 2017).…”

“…Their responses to vibration stimuli are characterized by on-phasic excitation to stimulus onset, tonic inhibition during continuous stimulation, and rebound spiking after vibration offset (Ai et al 2009). DL-Int-1 neurons are thought to play a central role in encoding the duration of the waggle phase (Ai et al 2017), which indicates the distance of the advertised food source from the hive (von Frisch 1993).…”