Network simulations of interneuron circuits in the honeybee primary auditory center

Abstract

Processing of airborne vibration signals in the auditory system is essential for honeybee 1 communication through the waggle dance language. Properties of neurons in the honeybee 2 primary auditory center suggest a circuitry of excitatory and inhibitory neurons encoding 3 these communication signals. To test this assumption, we simulated this network and 4 analyzed the predicted responses for different types of inputs. In particular, we investigated 5 the effect of specific inhibitory connections in the network. The results indicate that the 6 experimentally observed responses of certain interneuron types are compatible with an 7 inhibitory network of vibration processing in the primary auditory center of the honeybee. 8 Introduction 9Waggle dance and the honeybee primary auditory center 10 One of many fascinating behaviors of the honeybee is the "Waggle Dance", which is used 11 by returning forager honeybees to advertise the location of beneficial resources like food, 12 water and pollen among hive mates (Von Frisch 1967). The waggle dance consists of the 13 "waggle phase" during which the honeybee walks in a specific direction wagging its body 14 and flapping its wings, and a "return phase" during which it returns along a curved path to 15 the start of the waggle phase. The waggle phase represents the flight path of the bee from 16 the hive to resource, encoding the distance and direction of the resource in its duration 17 and orientation, respectively. During the waggle phase, body and wing movements of the 18 dancer honeybee produce pulses of air vibrations of specific frequency (≈265 Hz), duration 19 (≈16 ms) and inter-pulse-interval (≈33 ms) (Wenner 1962). These "sounds" are 20 important for successful recruitment of foragers (Barth et al. 2005;Michelsen 2003) and 21 are sensed by follower bees using the Johnston's Organ (JO) in their antennae. Sensory 22 neurons in the JO transduce air vibrations into neural signals (Tsujiuchi et al. 2007) and 23 convey them to the honeybee brain, specifically to the Dorsal Lobe (DL), the dorsal Sub 24 Esophageal ganglion (dSEG) and the medial Posterior Protocerebral Lobe (mPPL) (Ai 25 et al. 2009), the regions forming the primary auditory center (PAC) of the honeybee brain. 26

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

“…DL-Int-1 is GABAergic and likely part of a disinhibitory network (Ai et al 2017; Kumaraswamy et al 2017). Therefore, increased spontaneous rate and post-stimulus rebound in foragers compared to newly emerged adults is expected to result in enhanced strength of the inhibitory signal indicating antennal vibration.…”

“…Thus, the inhibitory response to vibration stimuli was relatively stronger in foragers than in newly emerged adults. Since DL-Int-1 is itself inhibitory and possibly part of a disinhibitory network (Ai et al 2017; Kumaraswamy et al 2017), this enhancement results in more effective disinhibition. Furthermore, the strength of postinhibitory rebound doubled during maturation.…”

“…These changes are likely due to maturation of the electrophysiological properties of DL-Int-1 as well as its connected neuronal network. Specifically, the adaptations in the strength of inhibition relative to spontaneous activity could have a stronger dependence on network factors as DL-Int-1 is inhibitory and is believed to be inhibited in turn as part of a disinhibitory network in the honeybee primary auditory center (Ai et al 2017; Kumaraswamy et al 2017). Clarification of the contribution of these two sources would be beneficial for further understanding the role of DL-Int-1 in networks that process waggle dance vibration signals in the primary auditory center of the honeybee.…”

“…These pulses are detected by follower bees, from which they learn about the location of food sources (Michelsen et al 1992; Landgraf 2013). There is evidence that DL-Int-1 plays a role in encoding the distance information from waggle dance airborne vibration patterns (Ai et al 2017; Kumaraswamy et al 2017). The observed changes indicate that, as the honeybee matures, there is refinement at structural and functional levels of the neurons and networks involved in processing the waggle dance communication signals that prepare the bees to process those important signals as foragers efficiently.…”

Inhibitory Pathways for Processing the Temporal Structure of Sensory Signals in the Insect Brain

“…In contrast, when trains of pulses with long-PP are applied to the antenna, DL-Int-1 shows intermittent spikes during the train of pulses ( Figure 1M , right column, asterisks), and DL-Int-2 often shows a lack of spikes with remarkable IPSPs ( Figure 1M , dots). A computational analysis based on these data suggests that the honeybee may use a disinhibitory network to encode the duration of the WP: DL-Int-2 spiking upon excitatory input from JO afferents is elicited by an inhibition of the presynaptic inhibitory neuron DL-Int-1 ( Figures 2E,F ; Kumaraswamy et al, 2017 ). Importantly, DL-Int-2 spikes in response to stimulation by trains of pulses with short PP ( Figure 1M , left), presumably as a result of the short-PP selectivity of the inhibition from DL-Int-1.…”