Context-dependent memory traces in the crab’s mushroom bodies: Functional support for a common origin of high-order memory centers

Abstract

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 reniform body: An integrative lateral protocerebral neuropil complex of Eumalacostraca identified in Stomatopoda and Brachyura

“…Finally, the reniform body's initial zone has no resemblance to a calyx. These observations are disparate to Maza et al () and interestingly these authors show compelling evidence that the N . granulata reniform body participates in context‐dependent visual memory.…”

“…Thus, as shown in Figure , all the topography of the mushroom body and reniform body in Stomatopoda correspond to those in shore crabs. This similarity strongly suggests that the center described by Maza et al () as a “mushroom body” in the crab N . granulata is neither a mushroom body nor its evolved modification, the hemiellipsoid body.…”

“…Finally, the reniform body's initial zone has no resemblance to a calyx. These observations are disparate to Maza et al (2016) and interestingly these authors show compelling evidence that the N. granulata reniform body participates in context-dependent visual memory. This observation, we would suggest, further aligns this center in the crab with our present observations of the stomatopod reniform body, demonstrating its unambiguous connections to the visual system's lobula and to the mushroom bodies.…”

“…Observations of Varunidae and Ocypodidae (fiddler crabs), which belong to Brachyura, the evolutionarily youngest reptantian clade (Wolfe et al, 2019), verified they also possess centers corresponding to the stomatopod reniform body. In the varunid crab Neohelice granulata, this center is of particular interest because of evidence that it participates in learning and memory, expressed as long-term habituation to noxious visual stimuli (Maza, Sztarker, Shkedy, Peszano, Locatelli, & Delorenzi, 2016).…”

Mushroom bodies in crustaceans: Insect‐like organization in the caridid shrimp Lebbeus groenlandicus

“…In contrast to these many differences of olfactory pathway organization, corresponding distinctions do not appear to pertain to the protocerebrum, where insect and eumalacostracan genera possess phenotypically corresponding mushroom bodies or their evolved derivatives that lack columnar extensions, that is, the hemiellipsoid bodies. One minor cause for confusion is that Stomatopoda and decapod Eumalacostraca also possess a second columnar neuropil in the lateral protocerebrum, called the reniform body, that serves the visual system in detecting and habituating to repetitive stimuli (Maza et al, ; Wolff et al, ). The correspondence of crustacean and insect protocerebra are also well supported with respect to the central complex neuropils and the protocerebrum's medial lobes (Thoen et al, ; Wolff et al, ).…”