skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: The reniform body: An integrative lateral protocerebralneuropil complex of Eumalacostraca identified in Stomatopodaand Brachyura
Mantis shrimps (Stomatopoda) possess in common with other crustaceans, and with Hexapoda, specific neuroanatomical attributes of the protocerebrum, the most anterior part of the arthropod brain. These attributes include assemblages of interconnected centers called the central body complex and in the lateral protocerebra, situated in the eyestalks, paired mushroom bodies. The phenotypic homologues of these centers across Panarthropoda support the view that ancestral integrative circuits crucial to action selection and memory have persisted since the early Cambrian or late Ediacaran. However, the discovery of another prominent integrative neuropil in the stomatopod lateral protocerebrum raises the question whether it is unique to Stomatopoda or at least most developed in this lineage, which may have originated in the upper Ordovician or early Devonian. Here, we describe the neuroanatomical structure of this center, called the reniform body. Using confocal microscopy and classical silver staining, we demonstrate that the reniform body receives inputs from multiple sources, including the optic lobe's lobula. Although the mushroom body also receives projections from the lobula, it is entirely distinct from the reniform body, albeit connected to it by discrete tracts. We discuss the implications of their coexistence in Stomatopoda, the occurrence of the reniform body in another eumalacostracan lineage and what this may mean for our understanding of brain functionality in Pancrustacea.  more » « less
Award ID(s):
1754610
PAR ID:
10183849
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
The Journal of comparative neurology
ISSN:
1096-9861
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Mantis shrimps (Stomatopoda) possess in common with other crustaceans, and with Hexapoda, specific neuroanatomical attributes of the protocerebrum, the most anterior part of the arthropod brain. These attributes include assemblages of interconnected centers called the central body complex and in the lateral protocerebra, situated in the eyestalks, paired mushroom bodies. The phenotypic homologues of these centers across Panarthropoda support the view that ancestral integrative circuits crucial to action selection and memory have persisted since the early Cambrian or late Ediacaran. However, the discovery of another prominent integrative neuropil in the stomatopod lateral protocerebrum raises the question whether it is unique to Stomatopoda or at least most developed in this lineage, which may have originated in the upper Ordovician or early Devonian. Here, we describe the neuroanatomical structure of this center, called the reniform body. Using confocal microscopy and classical silver staining, we demonstrate that the reniform body receives inputs from multiple sources, including the optic lobe's lobula. Although the mushroom body also receives projections from the lobula, it is entirely distinct from the reniform body, albeit connected to it by discrete tracts. We discuss the implications of their coexistence in Stomatopoda, the occurrence of the reniform body in another eumalacostracan lineage and what this may mean for our understanding of brain functionality in Pancrustacea. 
    more » « less
  2. Paired centers in the forebrain of insects, called the mushroom bodies, have become the most investigated brain region of any invertebrate due to novel genetic strategies that relate unique morphological attributes of these centers to their functional roles in learning and memory. Mushroom bodies possessing all the morphological attributes of those in dicondylic insects have been identified in mantis shrimps, basal hoplocarid crustaceans that are sister to Eumalacostraca, the most species-rich group of Crustacea. However, unless other examples of mushroom bodies can be identified in Eumalacostraca, the possibility is that mushroom body-like centers may have undergone convergent evolution in Hoplocarida and are unique to this crustacean lineage. Here, we provide evidence that speaks against convergent evolution, describing in detail the paired mushroom bodies in the lateral protocerebrum of a decapod crustacean, Lebbeus groenlandicus, a species belonging to the infraorder Caridea, an ancient lineage of Eumalacostraca. 
    more » « less
  3. Brain centers possessing a suite of neuroanatomical characters that define mushroom bodies of dicondylic insects have been identified in mantis shrimps, which are basal malacostracan crustaceans. Recent studies of the caridean shrimp Lebbeus groenlandicus further demonstrate the existence of mushroom bodies in Malacostraca. Nevertheless, received opinion promulgates the hypothesis that domed centers called hemiellipsoid bodies typifying reptantian crustaceans, such as lobsters and crayfish, represent the malacostracan cerebral ground pattern. Here, we provide evidence from the marine hermit crab Pagurus hirsutiusculus that refutes this view. P. hirsutiusculus, which is a member of the infraorder Anomura, reveals a chimeric morphology that incorporates features of a domed hemiellipsoid body and a columnar mushroom body. These attributes indicate that a mushroom body morphology is the ancestral ground pattern, from which the domed hemiellipsoid body derives and that the “standard” reptantian hemiellipsoid bodies that typify Astacidea and Achelata are extreme examples of divergence from this ground pattern. This interpretation is underpinned by comparing the lateral protocerebrum of Pagurus with that of the crayfish Procambarus clarkii and Orconectes immunis, members of the reptantian infraorder Astacidea. 
    more » « less
  4. Neural organization of mushroom bodies is largely consistent across insects, whereas the ancestral ground pattern diverges broadly across crustacean lineages resulting in successive loss of columns and the acquisition of domed centers retaining ancestral Hebbian-like networks and aminergic connections. We demonstrate here a major departure from this evolutionary trend in Brachyura, the most recent malacostracan lineage. In the shore crab Hemigrapsus nudus, instead of occupying the rostral surface of the lateral protocerebrum, mushroom body calyces are buried deep within it with their columns extending outwards to an expansive system of gyri on the brain’s surface. The organization amongst mushroom body neurons reaches extreme elaboration throughout its constituent neuropils. The calyces, columns, and especially the gyri show DC0 immunoreactivity, an indicator of extensive circuits involved in learning and memory. 
    more » « less
  5. Fiala, André; Meltzer, Hagar; Schleyer, Michael; Turrel, Oriane; Widmann, Annekathrin (Ed.)
    Associative memory in the Mushroom Body of the fruit fly brain depends on the encoding and processing of odorants in the first three stages of the Early Olfactory System: the Antenna, the Antennal Lobe and the Mushroom Body Calyx. The Kenyon Cells (KCs) of the Calyx provide the Mushroom Body compartments the identity of pure and odorant mixtures encoded as a train of spikes. Characterizing the code underlying the KC spike trains is a major challenge in neuroscience. To address this challenge we start by explicitly modeling the space of odorants using constructs of both semantic and syntactic information. Odorant semantics concerns the identity of odorants while odorant syntactics pertains to their concentration amplitude. These odorant attributes are multiplicatively coupled in the process of olfactory transduction. A key question that early olfactory systems must address is how to disentangle the odorant semantic information from the odorant syntactic information. To address the untanglement we devised an Odorant Encoding Machine (OEM) modeling the first three stages of early olfactory processing in the fruit fly brain. Each processing stage is modeled by Divisive Normalization Processors (DNPs). DNPs are spatio-temporal models of canonical computation of brain circuits. The end-to-end OEM is constructed as cascaded DNPs. By extensively modeling and characterizing the processing of pure and odorant mixtures in the Calyx, we seek to answer the question of its functional significance. We demonstrate that the DNP circuits in the OEM combinedly reduce the variability of the Calyx response to odorant concentration, thereby separating odorant semantic information from syntactic information. We then advance a code, called first spike sequence code, that the KCs make available at the output of the Calyx. We show that the semantics of odorants can be represented by this code in the spike domain and is ready for easy memory access in the Mushroom Body compartments. 
    more » « less