The hypothesis of a common origin for the high-order memory centers in bilateral animals is based on the evidence that several key features, including gene expression and neuronal network patterns, are shared across several phyla. Central to this hypothesis is the assumption that the arthropods' higher order neuropils of the forebrain [the mushroom bodies (MBs) of insects and the hemiellipsoid bodies (HBs) of crustaceans] are homologous structures. However, even though involvement in memory processes has been repeatedly demonstrated for the MBs, direct proof of such a role in HBs is lacking. Here, through neuroanatomical and immunohistochemical analysis, we identified, in the crab Neohelice granulata, HBs that resemble the calyxless MBs found in several insects. Using in vivo calcium imaging, we revealed training-dependent changes in neuronal responses of vertical and medial lobes of the HBs. These changes were stimulus-specific, and, like in the hippocampus and MBs, the changes reflected the context attribute of the memory trace, which has been envisioned as an essential feature for the HBs. The present study constitutes functional evidence in favor of a role for the HBs in memory processes, and provides key physiological evidence supporting a common origin of the arthropods' high-order memory centers.L earning skills vary across species depending upon specific adaptations to environmental features (1). However, beyond such adaptations, different species share many of the basic mechanisms involved in learning and memory. Both the molecular machinery involved in neural plasticity and the dynamics of the memory processes are conserved throughout evolution (2-5). This characteristic is critical to the hypothesis of a common origin of the high-order memory centers in bilateral animals (6, 7), centers that play a fundamental role in learning and memory by orchestrating high-order sensory processing within contextual frameworks (8, 9). The idea that these centers evolved from the same structure in a common ancestor has been reborn after the remarkable study of Tomer et al. (7) indicating deep homology of mushroom bodies (MBs) and the vertebrate pallium that dates back the origin of higher brain centers to the protostome-deuterostome ancestor times. The vertebrate pallium and the annelid MBs have a conserved overall molecular brain topology and neuron types (7). Furthermore, MBs and the hippocampus' dentate gyrus share the ability to generate new neurons during adult life (6,10,11). In this context, a recent study by Wolff and Strausfeld (6) has proposed that the similarities in both neuronal architectures and protein expression patterns between the mammalian hippocampus, the MBs, and the hemiellipsoid bodies (HBs) of crustaceans are important indicators of genealogical correspondence.MBs are complex paired structures of the forebrain of invertebrate species and have been vastly studied in insects (12). Since their description in the mid-1850s, the MBs have been considered higher order brain centers involved in memory...
The hypothesis of a common origin for high-order memory centers in bilateral animals presents the question of how different brain structures, such as the vertebrate hippocampus and the arthropod mushroom bodies, are both structurally and functionally comparable. Obtaining evidence to support the hypothesis that crustaceans possess structures equivalent to the mushroom bodies that play a role in associative memories has proved challenging. Structural evidence supports that the hemiellipsoid bodies of hermit crabs, crayfish and lobsters, spiny lobsters, and shrimps are homologous to insect mushroom bodies. Although a preliminary description and functional evidence supporting such homology in true crabs (Brachyura) has recently been shown, other authors consider the identification of a possible mushroom body homolog in Brachyura as problematic. Here we present morphological and immunohistochemical data in Neohelice granulata supporting that crabs possess well-developed hemiellipsoid bodies that are resolved as mushroom bodies-like structures. Neohelice exhibits a peduncle-like tract, from which processes project into proximal and distal domains with different neuronal specializations. The proximal domains exhibit spines and en passant-like processes and are proposed here as regions mainly receiving inputs. The distal domains exhibit a "trauben"-like compartmentalized structure with bulky terminal specializations and are proposed here as output regions. In addition, we found microglomeruli-like complexes, adult neurogenesis, aminergic innervation, and elevated expression of proteins necessary for memory processes. Finally, in vivo calcium imaging suggests that, as in insect mushroom bodies, the output regions exhibit stimulus-specific activity. Our results support the shared organization of memory centers across crustaceans and insects.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.