Context dependent memory traces in the crab's mushroom bodies: Functional support for a common origin of high order memory centers
Significance Mushroom bodies (MBs) are higher brain structures of several invertebrate groups, vastly studied in insects as a key structure involved in memory processes. Moreover, MBs and the vertebrate pallium have been proposed to share an ancestral common origin. In crustaceans, the hemiellipsoid bodies (HBs) are proposed to be homologues of the insect MBs. However, functional evidence for the involvement of HBs in memory processes is lacking. Here, in the crab Neohelice, we show memory traces in the HBs that, as for MBs, reflect the context attribute of memory. These results extend the homology based on anatomy and gene expression to the functional level. Consequently, present data support the hypothesis of a common origin for the arthropods' high order memory centers. 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.
Proceedings of the National Academy of Sciences