Regeneration of olfactory afferent axons in the locust brain

Abstract

The insect olfactory system consists of thousands of sensory neurons on each antenna, which project into the primary olfactory center, the glomerular antennnal lobe. There, they form synapses with local interneurons and projection neurons, which relay olfactory information to the second-order olfactory center, the mushroom body. Olfactory afferents of adult locusts (Locusta migratoria) were axotomized by crushing the base of the antenna. We studied the resulting degeneration and regeneration in the antennal lobe by size measurements, anterograde dye labeling through the antennal nerve, and immunofluorescence staining of cell surface markers. Within 3 days postcrush, the antennal lobe size was reduced by 30% and from then onward regained size back to normal by 2 weeks postinjury. Concomitantly, anterograde labeling revealed regenerating afferents reaching the antennal lobe by day 4 postcrush, and reinnervating the olfactory neuropil almost back to normal within 2 weeks. Regenerated fibers were directed precisely into the antennal lobe, where they reinnervated glomeruli. As a remarkable exception, a few regenerating fibers projected erroneously into the mushroom body on a pathway that is normally chosen by second-order projection neurons. Regenerating afferents expressed the cell surface proteins lachesin and fasciclin I. The antennal lobe neuropil expressed the cell surface marker semaphorin 1a. In conclusion, axonal regeneration in the locust olfactory system appears to be possible, precise, and fast, opening the possibility of future functional and mechanistic studies.

Scanning Laser Optical Tomography Resolves Structural Plasticity during Regeneration in an Insect Brain

“…Here, we adopted a novel OPT-technique, referred to as Scanning Laser Optical Tomography (SLOTy) [24], to follow structural changes in the brain of the model insect Locusta migratoria. Primary olfactory centers of the locust have the capacity to structurally regenerate upon sensory deafferentation [13]. In this study we showed that SLOTy can serve as a suitable method to rapidly illustrate and quantify neuronal plasticity of locust olfactory neuropils while maintaining the three dimensional structure of the brain.…”

“…Antennal lobes shrink after crushing the antennal nerve and regain size almost back to normal within 14 days [13]. Here we use SLOTy to follow size changes of the antennal lobe after unilateral nerve crush or antennal ablation over a period of 21 days.…”

“…Thus, basal mechanisms of neuronal regeneration can be studied in insect models without the need to overcome inhibitory extrinsic factors. We have recently introduced the olfactory pathway of the locust Locusta migratoria as a model system for neural regeneration demonstrating that axonal regeneration in this system is possible and beyond that, fast and precise [13].…”

Untethered Insect Interfaces

“…Specifically, fly studies have shown that the extension of retinal axons toward the brain is carried out in the early pupal phases, followed by a period of synaptogenesis in the midand late-pupal stages [53,54]. Moreover, a number of studies reported that damage to afferent processes extending from sensory organs to the brain were robust to rewiring or rerouting upon injury [50,[55][56][57]. Given this, we hypothesized that the introduction of perforated, sufficiently thin substrates (Figure 3.2a) normal to the plane of axonal extension in the mid-pupa phase (between 20 and 50% pupation) would allow for process innervation through that substrate and be robust to the injury of processes already present (i.e., damaged afferent processes might re-extend).…”

Lesion-induced insights in the plasticity of the insect auditory system

“…This cell surface molecule is expressed on probably all sensory axons of insects during embryogenesis (Bastiani et al, 1987); its expression is maintained in the adult nervous system in distinct sensory neuropil areas, but not in others (Jacobs and Lakes-Harlan, 2000). Upregulation of this molecule has been demonstrated in neuronal regeneration in the antennal system, but not yet for auditory axons (Stern et al, 2012). However, it has been documented that regenerating auditory afferents can follow Fasciclin I positive non-auditory axonal tracts (Jacobs and Lakes-Harlan, 2000).…”