A crabs' high‐order brain center resolved as a mushroom body‐like structure

Abstract

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.

Mushroom bodies and reniform bodies coexisting in crabs cannot both be homologs of the insect mushroom body

“…Reniform bodies and mushroom bodies are each defined by their own distinctive set of morphological traits (Table 1), those of reniform bodies identified from observations of Stomatopoda and the crab Hemigrapsus nudus (Thoen et al, 2020). Some of those traits are indeed recognized by Maza et al (2020) but interpreted as belonging to an insect‐like mushroom body. Invariant features of the reniform body morphology that might be mistaken for mushroom body traits include a dense group of quite small perikarya, numbering in the hundreds, situated on the dorsal surface of the lateral protocerebrum.…”

“…Confidence in this yardstick makes it possible to recognize even radical departures from the ground pattern and to detect possible misidentifications (Strausfeld & Sayre, 2021). A recent example of misidentification is exemplified by two papers claiming that in a species of Brachyura (crabs) the reniform body, as recognized in Stomatopoda, is homologous to the insect mushroom body (see, Maza et al, 2020; Maza, Sztarker, et al, 2016).…”

Shore crabs reveal novel evolutionary attributes of the mushroom body

“…As demonstrated previously and again here, large DC0-positive domains cover much of the varunid lateral protocerebrum, suggesting relatively enormous (for an arthropod) learning and memory neuropils (Strausfeld et al, 2020). The proposition that the reniform body is the crab’s mushroom body (Maza et al, 2016, 2020) is refuted by Golgi impregnations and 3-D reconstructions of the lateral protocerebrum demonstrating the reniform body as entirely distinct from the huge DC0-positive mushroom body adjacent to it ( Figure 11 ).…”

“…Historically, identifying a mushroom body homologue in the crab's brain has been problematic. Claims for homologous centers range from paired neuropils in the brain's second segment, the deutocerebrum, later attributed to the olfactory system (Bethe 1897), to an insistence that the crab's reniform body is a mushroom body (Maza et al, 2016(Maza et al, , 2020.…”

“…Historically, identifying a mushroom body homologue in the crab’s brain has been problematic. Claims for homologous centers range from paired neuropils in the brain’s second segment, the deutocerebrum, later attributed to the olfactory system (Bethe 1897), to an insistence that the crab’s reniform body is a mushroom body (Maza et al, 2016, 2020). Demonstrated 132 years ago in stomatopod crustaceans, the reniform body is a morphologically distinct center that coexists in the brain’s lateral protocerebrum adjacent to its columnar mushroom bodies (Bellonci, 1882; Thoen et al, 2019).…”