Identifying neuromodulatory input neurons to the fan-shaped body of the insect central complex

Abstract

Insects exhibit exceptional navigational abilities utilizing a compartment of their brain known as the central complex (CX). The CX comprises four distinct neuropils. These include the protocerebral bridge (PB), the fan-shaped body (FB), the ellipsoid body (EB) and the noduli (NO). Functionally, the CX has been implicated in encoding the insects current heading, its goal heading, and in instructing the insects steering decisions if these two angles do not match. Which goal heading is appropriate in any given situation depends on internal and external context, likely mediated via neuromodulatory input to the FB. The integration of directional information and contextual information in the FB thus forms the basis for context dependent action selection, providing different species with their unique behavioral repertoire. To reveal the concrete neural substrate of neuromodulatory input to the FB, we have performed volume electron microscopy based neural reconstructions of FB tangential neurons in the sweat bee (Megalopta genalis) as well as immunohistochemical labeling of neuromodulatory transmitters in the bumblebee (Bombus terrestris) and the hoverfly (Eristalis tenax). These include serotonin (5-HT), dopamine (labeling of tyrosin hydroxilase), Myoinhibitory peptide, FMRFamide, Gastrin/cholecystokinin, Crustacean Cardioactive peptide and Drosophila allatotropin/Lom-accessory gland-myotropin I. Labeling for these neuromodulators was confined to a limited set of tangential neurons in distinct FB layers. These were then matched with digital reconstruction from our connectomics data to obtain likely neural identities of neurons using modulating transmitters. Our results show that the layering of modulating transmitters in the bumblebee is different to that of the hoverfly but similar to the digital reconstructions in the sweat bee. Overall, our results are suited to shed light on the evolution of the neural circuits in the FB, illuminating conserved core circuit motifs as well as circuit aspects possibly involved in mediating species identity.

Popular Abstract

Insects have very different behaviours, including a great variety of navigational strategies. Although insects have many differences, they all have an almost identical navigation centre in the brain, which is called the central complex (CX). By exploring this brain region, we hope to discover how such great variety of navigational behaviour can be created by an almost identical brain region and therefore, the evolutionary and ecological adaptations in neural projections. In the fruit fly (Drosophila melanogaster), it is suggested that neurons in a compartment of the CX, named the fan-shaped body (FB), can modulate steering output cells in the CX in a context-dependent matter. These cells are called Fan-shaped body tangential (FBt) cells. This indicates that differences of FBt cells between species could hold critical information which could explain species behavioural repertoire. These neuromodulatory input neurons use modulatory transmitters, we hope to discover the identity of these in bumblebees (Bombus terrestris), and hoverflies (Eristalis tenax), since these species are quite far apart in evolution but have similar ecology.

We used immunohistochemistry to determine the expression profiles of seven neurotransmitters, including serotonin, and dopamine, as well as several neuropeptides. Each of those was expressed in specific layers of the FB, consistent with their presence in FBt neurons. The detailed shape and identity of those layers differed between the two tested species. Interestingly, the layers in which the FBt cells aborize in bumblebees are more alike those of locusts, which have an anterior - posterior division while the hoverflies have a horizontal organization. This implies that the layers in which the FBt cells aborize do not look more similar in more closely related species. Furthermore, the neurotransmitter profile varies even in closely related species. When we compare our immunohistochemical labelling to previous studies of the honeybee (Apis mellifera) it differs in that there is not any FMRFamide or gastrin in the CX of the bumblebee. This might be a factor in creating their various behaviours, hence their context dependent action selection.

We could distinguish neuronal tracts of FBt cells, and the layers in which they aborize from the immunohistochemical data. We used this information of the bumblebee to compare to digitalised FBt cells in the sweat bee (Megalopta genalis). The dopaminergic and serotonergic tracts in the bumblebee look highly similar to a ventral and an anterior digitalised neuronal tract, in the sweat bee. This indicates that we can assume the projection pattern of FBt cells with known neurochemistry in the bumblebee. This also means that we are one step closer to understanding the functioning of FBt cells and the creation of different behaviours across species.

• author: Langreiter, Matilda
• supervisor: Stanley Heinze
• organization: Degree Projects in Biology
• course: BION03 20241
• year: 2025
• type: H2 - Master's Degree (Two Years)
• subject: Biology and Life Sciences
• language: English
• id: 9186734
• date added to LUP: 2025-03-20 08:50:48
• date last changed: 2025-03-20 08:54:26