scholarly journals Shore crabs reveal novel evolutionary attributes of the mushroom body

2020 ◽  
Author(s):  
Nicholas James Strausfeld ◽  
Marcel Ethan Sayre

AbstractNeural 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. 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.

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Nicholas Strausfeld ◽  
Marcel E Sayre

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.


2019 ◽  
Author(s):  
Nicholas J. Strausfeld ◽  
Gabriella H. Wolff ◽  
Marcel E. Sayre

AbstractDescriptions of crustacean brains have mainly focused on three highly derived lineages: the reptantian infraorders represented by spiny lobsters, lobsters, and crayfish. Those descriptions advocate the view that dome- or cap-like neuropils, referred to as “hemiellipsoid bodies,” are the ground pattern organization of centers that are comparable to insect mushroom bodies in processing olfactory information. Here we challenge the doctrine that hemiellipsoid bodies are a derived trait of crustaceans, whereas mushroom bodies are a derived trait of hexapods. We demonstrate that mushroom bodies typify lineages that arose before Reptantia and exist in Reptantia. We show that evolved variations of the mushroom body ground pattern are, in some lineages, defined by extreme diminution or loss and, in others, by the incorporation of mushroom body circuits into lobeless centers. Such transformations are ascribed to modifications of the columnar organization of mushroom body lobes that, as shown in Drosophila and other hexapods, contain networks essential for learning and memory. We propose that lobed mushroom bodies distinguish crustaceans that negotiate the multidimensionality of complex ecologies, where continuous updating of multistimulus valence and memory is paramount.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Nicholas James Strausfeld ◽  
Gabriella Hanna Wolff ◽  
Marcel Ethan Sayre

Descriptions of crustacean brains have focused mainly on three highly derived lineages of malacostracans: the reptantian infraorders represented by spiny lobsters, lobsters, and crayfish. Those descriptions advocate the view that dome- or cap-like neuropils, referred to as ‘hemiellipsoid bodies,’ are the ground pattern organization of centers that are comparable to insect mushroom bodies in processing olfactory information. Here we challenge the doctrine that hemiellipsoid bodies are a derived trait of crustaceans, whereas mushroom bodies are a derived trait of hexapods. We demonstrate that mushroom bodies typify lineages that arose before Reptantia and exist in Reptantia thereby indicating that the mushroom body, not the hemiellipsoid body, provides the ground pattern for both crustaceans and hexapods. We show that evolved variations of the mushroom body ground pattern are, in some lineages, defined by extreme diminution or loss and, in others, by the incorporation of mushroom body circuits into lobeless centers. Such transformations are ascribed to modifications of the columnar organization of mushroom body lobes that, as shown in Drosophila and other hexapods, contain networks essential for learning and memory.


2018 ◽  
Author(s):  
Sandhya Mogily ◽  
Meenakshi VijayKumar ◽  
Sunil Kumar Sethy ◽  
Joby Joseph

AbstractThe European honeybee, Apis mellifera is the most common insect model system for studying learning and memory. We establish that the olfactory system of Apis dorsata, an Asian species of honeybee as an equivalent model to Apis mellifera to study physiology underlying learning and memory. We created an Atlas of the antennal lobe and counted the number of glomeruli in the antennal lobe of Apis dorsata to be around 165 which is similar to the number in the other honey bee species Apis mellifera and Apis florea. Apis dorsata was found to have five antenno-cerebral tracts namely mACT, lACT and 3 mlACTS which appear identical to Apis mellifera. Intracellular recording showed that the antennal lobe interneurons exhibit temporally patterned odor-cell specific responses. The neuritis of Kenyon cells with cell bodies located in a neighborhood in calyx retain their relative neighborhoods in the peduncle and alpha lobe forming a columnar organization in the mushroom body. Alpha lobe and the calyx of the mushroom body were innervated by extrinsic neurons with cell bodies in the lateral protocerebrum. A set of GABA positive cells in the lateral protocerebrum send their neurites towards alpha-lobe. Apis dorsata was amenable to olfactory conditioning and showed good learning and memory retention at 24 hours. They were amenable to massed and spaced conditioning and could distinguish trained odor from an untrained novel odor.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Gabriella Hannah Wolff ◽  
Hanne Halkinrud Thoen ◽  
Justin Marshall ◽  
Marcel E Sayre ◽  
Nicholas James Strausfeld

Mushroom bodies are the iconic learning and memory centers of insects. No previously described crustacean possesses a mushroom body as defined by strict morphological criteria although crustacean centers called hemiellipsoid bodies, which serve functions in sensory integration, have been viewed as evolutionarily convergent with mushroom bodies. Here, using key identifiers to characterize neural arrangements, we demonstrate insect-like mushroom bodies in stomatopod crustaceans (mantis shrimps). More than any other crustacean taxon, mantis shrimps display sophisticated behaviors relating to predation, spatial memory, and visual recognition comparable to those of insects. However, neuroanatomy-based cladistics suggesting close phylogenetic proximity of insects and stomatopod crustaceans conflicts with genomic evidence showing hexapods closely related to simple crustaceans called remipedes. We discuss whether corresponding anatomical phenotypes described here reflect the cerebral morphology of a common ancestor of Pancrustacea or an extraordinary example of convergent evolution.


2018 ◽  
Author(s):  
Radostina Lyutova ◽  
Maximilian Pfeuffer ◽  
Dennis Segebarth ◽  
Jens Habenstein ◽  
Mareike Selcho ◽  
...  

1.AbstractDopaminergic neurons in the brain of theDrosophilalarva play a key role in mediating reward information to the mushroom bodies during appetitive olfactory learning and memory. Using optogenetic activation of Kenyon cells we provide evidence that a functional recurrent signaling loop exists between Kenyon cells and dopaminergic neurons of the primary protocerebral anterior (pPAM) cluster. An optogenetic activation of Kenyon cells paired with an odor is sufficient to induce appetitive memory, while a simultaneous impairment of the dopaminergic pPAM neurons abolishes memory expression. Thus, dopaminergic pPAM neurons mediate reward information to the Kenyon cells, but in turn receive feedback from Kenyon cells. We further show that the activation of recurrent signaling routes within mushroom body circuitry increases the persistence of an odor-sugar memory. Our results suggest that sustained activity in a neuronal circuitry is a conserved mechanism in insects and vertebrates to consolidate memories.


2018 ◽  
Author(s):  
Jill R. Crittenden ◽  
Efthimios M. C. Skoulakis ◽  
Elliott. S. Goldstein ◽  
Ronald L. Davis

ABSTRACTMEF2 (myocyte enhancer factor 2) transcription factors are found in the brain and muscle of insects and vertebrates and are essential for the differentiation of multiple cell types. We show that in the fruitfly Drosophila, MEF2 is essential for normal development of wing veins, and for mushroom body formation in the brain. In embryos mutant for D-mef2, there was a striking reduction in the number of mushroom body neurons and their axon bundles were not detectable. D-MEF2 expression coincided with the formation of embryonic mushroom bodies and, in larvae, expression onset was confirmed to be in post-mitotic neurons. With a D-mef2 point mutation that disrupts nuclear localization, we find that D-MEF2 is restricted to a subset of Kenyon cells that project to the α/β, and γ axonal lobes of the mushroom bodies, but not to those forming the α’/β’ lobes. Our findings that ancestral mef2 is specifically important in dopamine-receptive neurons has broad implications for its function in mammalian neurocircuits.


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