The mushroom bodies – prominent brain centres of arthropods and annelids with enigmatic evolutionary origin

Loesel, Rudolf; Heuer, Carsten M.

doi:10.1111/j.1463-6395.2009.00422.x

Cited by 34 publications

(30 citation statements)

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“…Only small masses of neurons at the basal parts of the tentacles are found in the L. satsuma brain. We did not observe a mushroom body in the brain, which is a notable structure in vagile polychaetes [27]−[30]. The simple structure of the L. satsuma brain is probably due to the sessile lifestyle of this worm.…”

Section: Discussionmentioning

confidence: 59%

Neuroanatomy of the Vestimentiferan Tubeworm Lamellibrachia satsuma Provides Insights into the Evolution of the Polychaete Nervous System

2013

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Vestimentiferan tubeworms are marine invertebrates that inhabit chemosynthetic environments, and although recent molecular phylogenetic analyses have suggested that vestimentiferan tubeworms are derived from polychaete annelids, they show some morphological features that are different from other polychaetes. For example, vestimentiferans lack a digestive tract and have less body segments and comparative neuroanatomy can provide essential insight into the vestimentiferan body plan and its evolution. In the present study, we investigated the adult nervous system in the vestimentiferan Lamellibrachia satsuma using antibodies against synapsin, serotonin, FMRMamide and acetylated α-tubulin. We also examined the expressions of neural marker genes, elav and synaptotagmin to reveal the distribution of neuronal cell bodies. Brain anatomy shows simple organization in Lamellibrachia compared to other polychaetes. This simplification is probably due to the loss of the digestive tract, passing through the body between the brain and the subesophageal ganglion. In contrast, the ventral nerve cord shows a repeated organizational structure as in the other polychaetes, despite the absence of the multiple segmentation of the trunk. These results suggest that the brain anatomy is variable depending on the function and the condition of surrounding tissues, and that the formation of the rope ladder-like nervous system of the ventral nerve cord is independent from segmentation in polychaetes.

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Section: Discussionmentioning

confidence: 59%

Neuroanatomy of the Vestimentiferan Tubeworm Lamellibrachia satsuma Provides Insights into the Evolution of the Polychaete Nervous System

2013

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“…The results 1) reinforce much of the classic literature on adult nereidid neural architecture based on methylene blue staining, histologic reconstruction, electron microscopy, and neurophysiology; 2) reveal previously unknown peripheral nerve interconnections and aspects of parapodial muscle innervation; 3) promote the notion that Smith [28] overlooked variation in parapodial nerve architecture and the presence/absence of lateral nerves among his study taxa; and 4) determine the approximate stages of juvenile ontogeny by which key features of the cephalic nervous system become morphologically distinguishable. Examples of the latter include, first, portions of the stomatogastric system, consisting of the nerves and ganglia responsible for foregut innervation; second, the corpora pedunculata, prominent structures of the anterior brain thought to integrate information from the various cephalic sensory organs, and that are potential homologs of arthropod mushroom bodies [3,37]; and third, two pairs of ciliated sense organs: the chemosensory nuchal organs of the posterior head, and the poorly understood Langdon's organs of the anterior head.…”

Section: Introductionmentioning

confidence: 99%

Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

2010

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BackgroundMembers of Family Nereididae have complex neural morphology exemplary of errant polychaetes and are leading research models in the investigation of annelid nervous systems. However, few studies focus on the development of their nervous system morphology. Such data are particularly relevant today, as nereidids are the subjects of a growing body of "evo-devo" work concerning bilaterian nervous systems, and detailed knowledge of their developing neuroanatomy facilitates the interpretation of gene expression analyses. In addition, new data are needed to resolve discrepancies between classic studies of nereidid neuroanatomy. We present a neuroanatomical overview based on acetylated α-tubulin labeling and confocal microscopy for post-embryonic stages of Neanthes arenaceodentata, a direct-developing nereidid.ResultsAt hatching (2-3 chaetigers), the nervous system has developed much of the complexity of the adult (large brain, circumesophageal connectives, nerve cords, segmental nerves), and the stomatogastric nervous system is partially formed. By the 5-chaetiger stage, the cephalic appendages and anal cirri are well innervated and have clear connections to the central nervous system. Within one week of hatching (9-chaetigers), cephalic sensory structures (e.g., nuchal organs, Langdon's organs) and brain substructures (e.g., corpora pedunculata, stomatogastric ganglia) are clearly differentiated. Additionally, the segmental-nerve architecture (including interconnections) matches descriptions of other, adult nereidids, and the pharynx has developed longitudinal nerves, nerve rings, and ganglia. All central roots of the stomatogastric nervous system are distinguishable in 12-chaetiger juveniles. Evidence was also found for two previously undescribed peripheral nerve interconnections and aspects of parapodial muscle innervation.ConclusionsN. arenaceodentata has apparently lost all essential trochophore characteristics typical of nereidids. Relative to the polychaete Capitella, brain separation from a distinct epidermis occurs later in N. arenaceodentata, indicating different mechanisms of prostomial development. Our observations of parapodial innervation and the absence of lateral nerves in N. arenaceodentata are similar to a 19th century study of Alitta virens (formerly Nereis/Neanthes virens) but contrast with a more recent study that describes a single parapodial nerve pattern and lateral nerve presence in A. virens and two other genera. The latter study apparently does not account for among-nereidid variation in these major neural features.

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“…For example, molecular fingerprint data provide strong evidence for a homology of insect and annelid mushroom bodies [54]. This notion is supported by morphological data which demonstrate that the neuroarchitecture of the mushroom bodies of annelids is in many details identical to that of arthropods [24,52,55]. In addition, the presence of mushroom bodies has been demonstrated for a wide variety of errant polychaetes [28].…”

Section: Discussionmentioning

confidence: 95%

Lophotrochozoan neuroanatomy: An analysis of the brain and nervous system of Lineus viridis(Nemertea) using different staining techniques

2011

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BackgroundThe now thriving field of neurophylogeny that links the morphology of the nervous system to early evolutionary events relies heavily on detailed descriptions of the neuronal architecture of taxa under scrutiny. While recent accounts on the nervous system of a number of animal clades such as arthropods, annelids, and molluscs are abundant, in depth studies of the neuroanatomy of nemerteans are still wanting. In this study, we used different staining techniques and confocal laser scanning microscopy to reveal the architecture of the nervous system of Lineus viridis with high anatomical resolution.ResultsIn L. viridis, the peripheral nervous system comprises four distinct but interconnected nerve plexus. The central nervous system consists of a pair of medullary cords and a brain. The brain surrounds the proboscis and is subdivided into four voluminous lobes and a ring of commissural tracts. The brain is well developed and contains thousands of neurons. It does not reveal compartmentalized neuropils found in other animal groups with elaborate cerebral ganglia.ConclusionsThe detailed analysis of the nemertean nervous system presented in this study does not support any hypothesis on the phylogenetic position of Nemertea within Lophotrochozoa. Neuroanatomical characters that are described here are either common in other lophotrochozoan taxa or are seemingly restricted to nemerteans. Since detailed descriptions of the nervous system of adults in other nemertean species have not been available so far, this study may serve as a basis for future studies that might add data to the unsettled question of the nemertean ground pattern and the position of this taxon within the phylogenetic tree.

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The mushroom bodies – prominent brain centres of arthropods and annelids with enigmatic evolutionary origin

Cited by 34 publications

References 50 publications

Neuroanatomy of the Vestimentiferan Tubeworm Lamellibrachia satsuma Provides Insights into the Evolution of the Polychaete Nervous System

Neuroanatomy of the Vestimentiferan Tubeworm Lamellibrachia satsuma Provides Insights into the Evolution of the Polychaete Nervous System

Confocal analysis of nervous system architecture in direct-developing juveniles of Neanthes arenaceodentata (Annelida, Nereididae)

Lophotrochozoan neuroanatomy: An analysis of the brain and nervous system of Lineus viridis(Nemertea) using different staining techniques

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