Mushroom body evolution demonstrates homology and divergence across Pancrustacea

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.

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Mushroom Body Homology and Divergence across Pancrustacea

10.1101/856872 ◽

2019 ◽

Author(s):

Nicholas J. Strausfeld ◽

Gabriella H. Wolff ◽

Marcel E. Sayre

Keyword(s):

Learning And Memory ◽

Mushroom Body ◽

Mushroom Bodies ◽

Ground Pattern ◽

Olfactory Information ◽

Columnar Organization ◽

Spiny Lobsters

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.

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Shore crabs reveal novel evolutionary attributes of the mushroom body

eLife ◽

10.7554/elife.65167 ◽

2021 ◽

Vol 10 ◽

Author(s):

Nicholas Strausfeld ◽

Marcel E Sayre

Keyword(s):

Learning And Memory ◽

Mushroom Body ◽

Shore Crab ◽

Mushroom Bodies ◽

Evolutionary Trend ◽

Ground Pattern ◽

Neural Organization ◽

Shore Crabs ◽

Successive Loss ◽

Lateral Protocerebrum

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.

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Shore crabs reveal novel evolutionary attributes of the mushroom body

10.1101/2020.11.06.371492 ◽

2020 ◽

Author(s):

Nicholas James Strausfeld ◽

Marcel Ethan Sayre

Keyword(s):

Learning And Memory ◽

Mushroom Body ◽

Mushroom Bodies ◽

Evolutionary Trend ◽

Ground Pattern ◽

Neural Organization ◽

Shore Crabs ◽

Successive Loss ◽

Lateral Protocerebrum

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.

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An insect-like mushroom body in a crustacean brain

eLife ◽

10.7554/elife.29889 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 25

Author(s):

Gabriella Hannah Wolff ◽

Hanne Halkinrud Thoen ◽

Justin Marshall ◽

Marcel E Sayre ◽

Nicholas James Strausfeld

Keyword(s):

Spatial Memory ◽

Learning And Memory ◽

Sensory Integration ◽

Mushroom Body ◽

Convergent Evolution ◽

Visual Recognition ◽

Common Ancestor ◽

Mushroom Bodies ◽

Morphological Criteria

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.

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Reward signaling in a recurrent circuit of dopaminergic neurons and Kenyon cells

10.1101/357145 ◽

2018 ◽

Author(s):

Radostina Lyutova ◽

Maximilian Pfeuffer ◽

Dennis Segebarth ◽

Jens Habenstein ◽

Mareike Selcho ◽

...

Keyword(s):

Learning And Memory ◽

Dopaminergic Neurons ◽

Mushroom Body ◽

Olfactory Learning ◽

Mushroom Bodies ◽

Neuronal Circuitry ◽

Sustained Activity ◽

Kenyon Cells ◽

Reward Information ◽

The Brain

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.

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Olfactory Learning in Drosophila

Physiology ◽

10.1152/physiol.00026.2010 ◽

2010 ◽

Vol 25 (6) ◽

pp. 338-346 ◽

Cited By ~ 83

Author(s):

Germain U. Busto ◽

Isaac Cervantes-Sandoval ◽

Ronald L. Davis

Keyword(s):

Dopaminergic Neurons ◽

Mushroom Body ◽

Sensory Information ◽

Brain Regions ◽

Olfactory Learning ◽

Mushroom Bodies ◽

Neural Pathways ◽

Olfactory Information ◽

Appetitive Stimuli ◽

The Brain

Studies of olfactory learning in Drosophila have provided key insights into the brain mechanisms underlying learning and memory. One type of olfactory learning, olfactory classical conditioning, consists of learning the contingency between an odor with an aversive or appetitive stimulus. This conditioning requires the activity of molecules that can integrate the two types of sensory information, the odorant as the conditioned stimulus and the aversive or appetitive stimulus as the unconditioned stimulus, in brain regions where the neural pathways for the two stimuli intersect. Compelling data indicate that a particular form of adenylyl cyclase functions as a molecular integrator of the sensory information in the mushroom body neurons. The neuronal pathway carrying the olfactory information from the antennal lobes to the mushroom body is well described. Accumulating data now show that some dopaminergic neurons provide information about aversive stimuli and octopaminergic neurons about appetitive stimuli to the mushroom body neurons. Inhibitory inputs from the GABAergic system appear to gate olfactory information to the mushroom bodies and thus control the ability to learn about odors. Emerging data obtained by functional imaging procedures indicate that distinct memory traces form in different brain regions and correlate with different phases of memory. The results from these and other experiments also indicate that cross talk between mushroom bodies and several other brain regions is critical for memory formation.

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