Visual inputs to the mushroom body calyces of the whirligig beetle Dineutus sublineatus: Modality switching in an insect

Abstract

The mushroom bodies are prominent lobed centers in the forebrain, or protocerebrum, of most insects. Previous studies on mushroom bodies have focused on higher olfactory processing, including olfactory-based learning and memory. Anatomical studies provide strong support that in terrestrial insects with mushroom bodies, the primary input region, or calyces, are predominantly supplied by olfactory projection neurons from the antennal lobe glomeruli. In aquatic species that generally lack antennal lobes, the calyces are vestigial or absent. Here we report an exception to this in the whirligig beetle Dineutus sublineatus (Coleoptera: Gyrinidae). This aquatic species lives on water and is equipped with two separate pairs of compound eyes, one pair viewing above and one viewing below the water surface. As in other aquatic insects, the whirligig beetle lacks antennal lobes, but unlike other aquatic insects its mushroom bodies possess robust calyces. Golgi impregnations and fluorescent tracer injections revealed that the calyces are exclusively supplied by visual neurons from the medulla of the dorsal eye optic lobes. No other sensory inputs reach the calyces, thereby showing a complete switch of calyx modality from olfaction to vision. Potential functions of the mushroom bodies of D. sublineatus are discussed in the context of the behavioral ecology of whirligig beetles.

Evolution of brain elaboration

“…R. Soc. B 370: 20150054 the optic lobes to the calyces are also been described in dragonflies [76], the cockroach Periplaneta americana [77,78], the butterfly Pieris rapae [79] and the whirligig beetle Deineutus sublineatus [27]. In most of these insects, the mushroom bodies are large with expanded, often duplicated calyces, much like the mushroom bodies of the social Hymenoptera.…”

“…Interestingly, these structures do not appear to be capable of adapting to a return to an aquatic lifestyle, as olfactory bulbs and antennal lobes are lost or greatly reduced in secondarily aquatic animals such as cetaceans or whirligig beetles [26,27].…”

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

“…Fills into the receptor axons were of 2 h duration, after which whole-cell patch-clamp recording of the GDN culminated in filling it with biocytin, which was subsequently labeled with Streptavidin:Cy3. Using a method described previously by Lin and Strausfeld (Lin and Strausfeld, 2012), after they had been fixed in buffered paraformaldehyde and washed in phosphate buffer, brains were dehydrated, embedded in Spurr's resin (Electron Microscopy Science, Hatfield, PA, USA), sectioned at 20 μm and then mounted in Permount (Fisher Scientific, Fair Lawn, NJ, USA) under thin glass coverslips. Serial sections were scanned with a Zeiss Pascal three-line confocal microscope at increments of 1 μm.…”

Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

“…An interesting aspect is the fact that in some insects the mushroom bodies have been found to process visual input, either as part of a complete modality switch (Lin and Strausfeld, 2012) or by topographical division of the different modalities into separate areas (Kinoshita et al, 2014). The distinct projections of olfactory neurons into the outer layers of the hemiellipsoid body in stomatopods could suggest that the inner core could have a different function, perhaps processing visual information?…”

“…These hemiellipsoid bodies have been suggested to be homologues of the mushroom bodies in insects and morphology, ultrastructure and immunoreactivity advocate the same (Wolff et al, 2012). Recent studies have also revealed that the mushroom bodies are capable of modality switching, processing visual information instead of olfactory information in aquatic species which generally lack antennal lobes (Lin and Strausfeld, 2012).…”