The “amphi”-brains of amphipods: new insights from the neuroanatomy of Parhyale hawaiensis (Dana, 1853)

Abstract

Background Over the last years, the amphipod crustacean Parhyale hawaiensis has developed into an attractive marine animal model for evolutionary developmental studies that offers several advantages over existing experimental organisms. It is easy to rear in laboratory conditions with embryos available year-round and amenable to numerous kinds of embryological and functional genetic manipulations. However, beyond these developmental and genetic analyses, research on the architecture of its nervous system is fragmentary. In order to provide a first neuroanatomical atlas of the brain, we investigated P. hawaiensis using immunohistochemical labelings combined with laser-scanning microscopy, X-ray microcomputed tomography, histological sectioning and 3D reconstructions. Results As in most amphipod crustaceans, the brain is dorsally bent out of the body axis with downward oriented lateral hemispheres of the protocerebrum. It comprises almost all prominent neuropils that are part of the suggested ground pattern of malacostracan crustaceans (except the lobula plate and projection neuron tract neuropil). Beyond a general uniformity of these neuropils, the brain of P. hawaiensis is characterized by an elaborated central complex and a modified lamina (first order visual neuropil), which displays a chambered appearance. In the light of a recent analysis on photoreceptor projections in P. hawaiensis , the observed architecture of the lamina corresponds to specialized photoreceptor terminals. Furthermore, in contrast to previous descriptions of amphipod brains, we suggest the presence of a poorly differentiated hemiellipsoid body and an inner chiasm and critically discuss these aspects. Conclusions Despite a general uniformity of amphipod brains, there is also a certain degree of variability in architecture and size of different neuropils, reflecting various ecologies and life styles of different species. In contrast to other amphipods, the brain of P. hawaiensis does not display any striking modifications or bias towards processing one particular sensory modality. Thus, we conclude that this brain represents a common type of an amphipod brain. Considering various established protocols for analyzing and manipulating P. hawaiensis , this organism is a suitable model to gain deeper understanding of brain anatomy e.g. by using connectome approaches, and this study can serve as first solid basis for following studies. Electronic supplementary material The online version of this article (10.1186/s12983-019-0330-0) contains supplementary material, which is available to authorized users.

Masters of communication: The brain of the banded cleaner shrimp Stenopus hispidus (Olivier, 1811) with an emphasis on sensory processing areas

“…Conversely, the regionalization of the lateral flagellum into a proximal aesthetasc region can also be arranged like in spiny lobsters (Achelata), in which only the distal part of the lateral flagellum bears aesthetascs (Grünert & Ache, ). The bilobed structure of the associated lateral antennular neuropil as a feature of the malacostracan brain ground plan (Hanström, ; Kenning et al, ) was shown for Leptostraca (Kenning et al, ), Stomatopoda (Derby et al, ), Caridea, Euphausiacea, Anaspidacea, Eureptantia, (Sandeman et al, , ; Sandeman & Scholtz, ), and also Amphipoda (Ramm & Scholtz, ; Wittfoth, Harzsch, Wolff, & Sombke, ) but seems to be absent in members of the Isopoda (Harzsch et al, ; Kenning & Harzsch, ). In these isopods, the antennule is uniramous, suggesting that a biramous antennule is represented in a bilobed lateral antennular neuropil like in S. hispidus where each sublobe (lLAN and mLAN) is connected to an individual nerve (Harzsch et al, ; Kenning & Harzsch, ).…”

Mushroom bodies in Reptantia reflect a major transition in crustacean brain evolution

“…Like mushroom bodies, hemiellipsoid bodies receive inputs from deutocerebral olfactory neuropils and can, as will be show here, express elevated levels of DC0. However, despite the identification of mushroom bodies in malacostracans that are outgroups of decapods, contemporary accounts of decapod brains nevertheless define hemiellipsoid bodies as crustacean apomorphies and state, categorically, that these structures are established elements of the cerebral ground pattern of Malacostraca (Kenning, Müller, Wirkner, & Harzsch, ; Wittfoth, Harzsch, Wolff, & Sombke, ).…”

Mushroom Body Homology and Divergence across Pancrustacea

“…Fig. 12), stifles any discussion about evolution, as does the assertion of the hemiellipsoid body's ground pattern status, even in species where the neuropil is not demonstrable (Wittfoth et al, 2019). The recent demonstration of mushroom bodies in the Stomatopoda and other lineages described here present evidence that the mushroom bodies provide the ground pattern for the crustacean protocerebral olfactory center.…”

“…In his extensive 1931 study of decapod brains, Hanström stated throughout that hemiellipsoid bodies are mushroom bodies that either lack the columnar lobe or have incorporated it. Yet, in the ensuing years the belief that the domed hemiellipsoid bodies of crustaceans are fundamentally different structures from the lobed mushroom bodies of insects has become not only widely accepted, but specifically advocated as a basis for the ground pattern of the malacostracan brain (Sandeman et al, 2014;Wittfoth et al, 2019;Machon et al, 2019). The doctrine has become entrenched: that hemiellipsoid bodies are a derived trait of crustaceans, whereas mushroom bodies are a derived trait of hexapods (Sandeman et al, 2014;Machon et al, 2019).…”

“…The antibody, known as "anti-DC0", selectively identifies the columnar neuropils of mushroom bodies of insects (Farris and Strausfeld, 2003) and of other arthropods with, until very recently, the notable exception of crustaceans . Indeed, numerous studies have disputed or expressed ambivalence about centers in comparable locations in the crustacean brain being mushroom body homologues (e.g., Strausfeld et al, 1998;Fanenbruck et al, 2004;Fanenbruck and Harzsch, 2005;Farris, 2013;Sandeman et al, 2014;Krieger et al, 2015;Harzsch and Krieger, 2018;Machon et al, 2019;Wittfoth et al, 2019).…”