Genealogical correspondence of a forebrain centre implies an executive brain in the protostome–deuterostome bilaterian ancestor

Wolff, Gabriella H.; Strausfeld, Nicholas J.

doi:10.1098/rstb.2015.0055

Cited by 51 publications

(74 citation statements)

References 137 publications

(195 reference statements)

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“…the MB function, the HB has been largely predicted as a high-order memory center (6,25,26). However, to the extent of our knowledge, there is yet no direct evidence in favor of the occurrence of learning and memory processes in this neuropil.…”

mentioning

confidence: 94%

“…Both the molecular machinery involved in neural plasticity and the dynamics of the memory processes are conserved throughout evolution (2)(3)(4)(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.…”

mentioning

confidence: 99%

“…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.…”

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confidence: 99%

“…Moreover, HBs also generate new neurons during adult life (20,21). The concordance among several types of data, including topology, topography, gene expression, and functions, are useful to support phylogenic and/or structural homologies in the central nervous system (6,(22)(23)(24). Based on solid evidence about Significance Mushroom bodies (MBs) are higher brain structures of several invertebrate groups, vastly studied in insects as a key structure involved in memory processes.…”

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confidence: 99%

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

Maza

Sztarker

Shkedy

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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...

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mentioning

confidence: 94%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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

Maza

Sztarker

Shkedy

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…In their comparisons of arthropod and vertebrate brains, Wolff & Strausfeld [31] identify numerous structural, molecular and genetic characters that are shared by the vertebrate hippocampus and the arthropod mushroom bodies. The correspondences include a neuronal ground pattern that defines these forebrain structures and their ancestral relationships with the olfactory system.…”

Section: Organization and Contributions To This Issuementioning

confidence: 99%

Introduction to ‘Homology and convergence in nervous system evolution’

Strausfeld

Hirth

2016

Phil. Trans. R. Soc. B

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The origin of brains and central nervous systems (CNSs) is thought to have occurred before the Palaeozoic era 540 Ma. Yet in the absence of tangible evidence, there has been continued debate whether today's brains and nervous systems derive from one ancestral origin or whether similarities among them are due to convergent evolution. With the advent of molecular developmental genetics and genomics, it has become clear that homology is a concept that applies not only to morphologies, but also to genes, developmental processes, as well as to behaviours. Comparative studies in phyla ranging from annelids and arthropods to mammals are providing evidence that corresponding developmental genetic mechanisms act not only in dorso–ventral and anterior–posterior axis specification but also in segmentation, neurogenesis, axogenesis and eye/photoreceptor cell formation that appear to be conserved throughout the animal kingdom. These data are supported by recent studies which identified Mid-Cambrian fossils with preserved soft body parts that present segmental arrangements in brains typical of modern arthropods, and similarly organized brain centres and circuits across phyla that may reflect genealogical correspondence and control similar behavioural manifestations. Moreover, congruence between genetic and geological fossil records support the notion that by the ‘Cambrian explosion’ arthropods and chordates shared similarities in brain and nervous system organization. However, these similarities are strikingly absent in several sister- and outgroups of arthropods and chordates which raises several questions, foremost among them: what kind of natural laws and mechanisms underlie the convergent evolution of such similarities? And, vice versa: what are the selection pressures and genetic mechanisms underlying the possible loss or reduction of brains and CNSs in multiple lineages during the course of evolution? These questions were addressed at a Royal Society meeting to discuss homology and convergence in nervous system evolution. By integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, the meeting covered disparities in nervous system origins as well as correspondences of neural circuit organization and behaviours, all of which allow evidence-based debates for and against the proposition that the nervous systems and brains of animals might derive from a common ancestor.

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Nomen est omen, cognitive dissonance, and homology of memory centers in crustaceans and insects

Strausfeld

2020

J of Comparative Neurology

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In 1882, the Italian embryologist Giuseppe Bellonci introduced a nomenclature for structures in the stomatopod crustacean Squilla mantis that he claimed correspond to insect mushroom bodies, today recognized as cardinal centers that in insects mediate associative memory. The use of Bellonci's terminology has, through a series of misunderstandings and entrenched opinions, led to contesting views regarding whether centers in crustacean and insect brains that occupy corresponding locations and receive comparable multisensory inputs are homologous or homoplasic. The following describes the fate of terms used to denote sensory association neuropils in crustacean species and relates how those terms were deployed in the 1920s and 1930s by the Swedish neuroanatomist Bertil Hanström to claim homology in insects and crustaceans. Yet the same terminology has been repurposed by subsequent researchers to promote the very opposite view: that mushroom bodies are a derived trait of hexapods and that equivalent centers in crustaceans evolved independently.

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Genealogical correspondence of a forebrain centre implies an executive brain in the protostome–deuterostome bilaterian ancestor

Cited by 51 publications

References 137 publications

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

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

Introduction to ‘Homology and convergence in nervous system evolution’

Nomen est omen, cognitive dissonance, and homology of memory centers in crustaceans and insects

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